The Rate of Asymptomatic Throat Carriage of Streptococcus pyogenes and its Associated Risk Factors among Medical Students of Queen Arwa University in Sana’a City, Yemen

doi:10.21203/rs.3.rs-3121190/v1

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The Rate of Asymptomatic Throat Carriage of Streptococcus pyogenes and its Associated Risk Factors among Medical Students of Queen Arwa University in Sana’a City, Yemen

https://doi.org/10.21203/rs.3.rs-3121190/v1

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Background

Throat carriage of Streptococcus pyogenes could play a crucial role in the transmission of infection to households and community settings. In Yemen, there is no information about S. pyogenes throat carriage among university students.

Aim

This study aimed for finding out the rate of asymptomatic throat carriage of Streptococcus pyogenes and its associated risk factors among medical students of Queen Arwa University in Sana’a City, Yemen.

Methods

This cross-sectional study was conducted at Queen Arwa, between December 2022 to April 2023. A total of 300 throat swabs were randomly collected from medical university students. Streptococcus pyogenes were isolated and identified by using standard bacteriological procedures. Also, the required data were obtained by using the designed questionnaire.

Results

Out of 300 specimens, 5(1.7%) were positive for S. pyogenes throat carriage. The high rate of S. pyogenes was among females (2%), age group of 25–30 years (8.3%), dental students (3.9%), and who studied at the third level (3.7%). Also, the high rate of the carriage was whose fathers’ are the trading field (3.7%) and mothers as housewives (2%), whose fathers and mothers’ held a university certificate (2.9%) and primary school (6.5%), respectively, with a low income (12.5%), none of their families has a sore throat (2.1%), and a history of hospitalization (3.2%).

Conclusion

There was a relatively low rate of S. pyogenes throat carriage in healthy medical students compared with international investigations. Standard precautions such as adequate hand and respiratory hygiene and avoiding overcrowded settings are used to prevent and control transmission of GAS infection.

General Microbiology

Infectious Diseases

Epidemiology

Asymptomatic

Medical Students

Streptococcus pyogenes

Throat Carriage

Sana’a

Yemen

Streptococcus pyogenes (S. pyogenes), also called group A streptococcus (GAS), is a gram-positive, beta-hemolytic bacterium in the genus Streptococcus. S. pyogenes is the major human pathogen that colonizes epithelial and mucosal tissues. It causes several diseases varying from mild including skin and upper respiratory tract infections to severe life-threatening conditions such as rheumatic fever, glomerulonephritis, septicemia, pneumonia, and streptococcal toxic shock syndrome [1, 2].

S. pyogenes transmission occurs largely through droplets resulting from respiratory secretions. Also, it spreads through direct contact with secretions such as saliva, wound discharge, or nasal secretions, from an infected person. People with GAS pharyngitis are much more likely to transmit the bacteria to others than asymptomatic pharyngeal carriers [2].

Globally, the burden from S. pyogenes is estimated to be 33 million cases of severe disease and more than 600 000 deaths each year [3]. The high burden is particularly occurring in limited resources countries due to overcrowding conditions, inadequate personal hygiene, and lack of health awareness. Experts estimate that S. pyogenes causes 20–30% of pharyngitis incidents in children. In comparison, experts estimate it causes approximately 5–15% of pharyngitis infections in adults However, in adults, GAS pharyngitis will typically occur before the age of 40 and decline steadily after that [4].

S. pyogenes can colonies the oropharynx without causing any signs of disease; this is known as an asymptomatic carriage. Individuals who asymptomatically S. pyogenes carriage could play a role in the spread of infection to households and community settings, particularly environments where large crowds get together such as schools, universities, daycare centers, and offices [5, 6]. The S. pyogenes carriage rate among children can be over 10%, while in adults the reported carriage rate is much lower [7].

According to the previous studies conducted among adult students in some countries, the prevalence rate of S. pyogenes throat carriage was reported at 2–46% in Turkey [8], 9.6% in Philadelphia [9], 15.6% in Poland [10], 11.2–34% in India [11], 3.6% in Cyprus [5], and 16.9% in Kabul university [12].

In developing nations such as Yemen, overcrowding conditions, lack of health awareness, food insecurity, widespread poverty, and limited access to health services contribute to the prevalence of preventable diseases in the community [13–16]. Most of earlier studies which conducted in Ymene focused the S. pyogenes among children [6, 17]. Furthermore, there is no previous study regarding the asymptomatic carriage of S. pyogenes among university students in Yemen. So, the present study aimed for finding out the rate of asymptomatic throat carriage of S. pyogenes and its associated risk factors among medical students of Queen Arwa University in Sana’a City, Yemen.

Study area and period

This cross-sectional study was carried out among medical university students studying in the Faculty of Medical Sciences, Queen Arwa University (QAU), Sana’a City, Yemen between December 2022 to April 2023.

Study population

The study population was medical university students aged between 18–30 years. The participants are attending four medical departments including laboratory, pharmacy, dental, and therapeutic nutrition in QAU during the study period.

Sample size

The sample size was calculated by using Epi Info 7 (version 7.2.5) as the subsequent: The total size of medical students is 1593 registered in QAU. According to previous reports, the expected prevalence of S. pyogenes prevalence was 10.03% [5, 9, 12]. Also, 5% and 5% were set as an acceptable margin of error and confidence level, respectively. So, the required sample size for this study was 208 on program calculation. The sample size was raised to 300 to obtain more accurate results

Information collection

The needed information was collected by using a questionnaire. The demographic and socio-economic characterizations such as gender, age, major field of study, study level, parents’ job, parents’ education level, monthly income, housing, number of individuals per room, number of children in household, sharing clothes, towels, and shaving tools, fever, cough, suffering from heart rheumatism, receive treatment for rheumatic heart, one of your family had an upper respiratory infection, infected with skin rash due to sore throat previously, and history of hospitalization was gathered by via face-to-face interview and recorded in the questionnaire.

Inclusion and exclusion criteria

The inclusion criteria were all study participants who signed the consent inform, provide a throat swab, had no signs of GAS pharyngitis, and didn’t use antimicrobial drugs in the days before sampling. Medical university students were excluded from the study if they showed an infection in the upper respiratory tract, sore throat, or antibiotic usage within two weeks before sample collection.

Specimen size and collection

The swab specimens were collected with a sterile cotton swab that was swabbed from the upper tonsil and posterior pharyngeal areas. Sampled swabs were labeled with participated data and immediately transported (within 1 h) to the medical microbiology lab. in the QAU for microbiology examination.

Isolation and identification of S. pyogenes

The collected swabs were immediately inoculated on a blood agar plate (counting 5% sheep blood) (HiMedia Lab., India) by rolling the swab over an area of the plate and streaking and stabbing the sample using a sterile loop. The inoculated plates were incubated at 37°C with a 5% CO₂ atmosphere between 24–48 h. The beta-haemolytic colonies were confirmed for their sensitivity to bacitracin. Also, gram stain and biochemical tests were subjected to further purification [18].

Ethical considerations

The ethical approval of this project was permitted by the Ethics Committee of Queen Arwa University. Prior to data and specimen collection, the purposes of the study were well explained to the medical students to agree to their inclusion in this study. Participation in the work was voluntary and participants gave their informed written consent.

Statistical analysis

The results were statistically analyzed by using SPSS program version 26 (IBM SPSS Inc., Chicago., USA). Figures and tablets were prepared for presenting variables in categories in frequencies and percentages. The Chi-square test (χ2) was used for verifying the existence of associations. P-values ≤ 0.05 were considered statistically significant.

Socio-demographic characteristics

Out of 300 medical students who participated in the present study, 150(50% in each) were males and females, 276 (92%) were within the age of 18–24 years, dental students (42%), and studied at the third level (27.3%). In addition, 153 (51%) participant’s fathers were employees, 253 (84.3%) students’ mothers were a house-wife, 137 (45.7%) participants’ fathers were found to have universities certificate, 83(27.7%) students’ mothers had secondary school certificate, and 243(81%) participants had a middle monthly income (Table 1).

Table 1. Socio-demographic characters of study subjects

Variables		No. examined	Percentage (%)
Gender	Male	150	50
Gender	Female	150	50
Age group (in years)	18–24	276	92
Age group (in years)	25–30	24	8
Major field of study	Laboratory	61	20.3
	Pharmacy	71	23.7
	Dental	126	42.0
	Therapeutic Nutrition	42	14.0
Study level	Frist	60	20.0
	Second	69	23.0
	Third	82	27.3
	Fourth	55	18.3
	Fifth	34	11.3
Father job	Employee	153	51.0
	Trading	27	9.0
	Farmer	8	2.7
	Other	112	37.3
Mother's job	Employee	42	14.0
	Trading	2	.7
	Farmer	3	1.0
	Housewife	253	84.3
	Other	0	0
Education level for Father	Illiterate	24	8.0
	Primary	23	7.7
	Intermediate	27	9.0
	Secondary	89	29.7
	University	137	45.7
Education level for Mother	Illiterate	76	25.3
	Primary	46	15.3
	Intermediate	51	17.0
	Secondary	83	27.7
	University	44	14.7

Prevalence of S. pyogenes carriage

This result revealed that the overall rate of S. pyogenes carriage among university students was 5 (1.7%) while 295 (98.3%) was negative for S. pyogenes (Fig. 1).

Prevalence of S. pyogenes carriage concerning socio-demographic

This finding found that the high rate of S. pyogenes carriage among females participating (2%), age group of 25–30 years old (8.3%; P = 0.008), dental students (3.9%), and who studied at the third level (3.7%) (Table 2).

Table (2) Distribution of S. pyogenes carriage concerning socio-demographic

Variables		F. (%)	GAS		χ²	P- value
Variables		F. (%)	+ve (%)	–ve (%)	χ²	P- value
Gender	Male	150(50)	2(1.3)	149(98.7)	0.203	0.653
Gender	Female	150(50)	3(2)	146(98)	0.203	0.653
Age group (in years)	18–24	276(92)	3(1.1)	273(98.9)	7.074	0.008
Age group (in years)	25–30	24(8)	2(8.3)	22(91.7)	7.074	0.008
Major field of study	Laboratory	61(20.3)	0(0)	61(100)	7.022	0.071
	Pharmacy	71(23.7)	0(0)	71(100)
	Dental	126(42)	5(3.9)	121(96.1)
	Therapeutic nutrition	42(14)	0(0)	42(100)
Study level	Frist	60(20)	0(0)	60(100)	6.050	0.197
	Second	69(23)	0(0)	69(100)
	Third	82(27.3)	3(3.7)	79(96.3)
	Fourth	55(18.3)	2(3.6)	53(96.4)
	Fifth	34(11.3)	0(0)	34(100)

Significant statistics at P-value < 0.05. χ² = Chi-square test.

Prevalence of S. pyogenes concerning parent’s education and job

Table 3 shows the high rate of throat carriage of S. pyogenes among medical students whose fathers’ and mothers’ jobs are working in the trading field (3.7%) and only housewives (2%), respectively, with non-significant differences (P> 0.05). Also, the higher rate of S. pyogenes among medical students whose fathers held a university certificate (2.9%) and whose mothers held a primary school certificate (6.5%; P= 0.038). In addition, according to monthly income, the medical university students with a low income had the highest rate of S. pyogenes carriage (12.5%) while the lowest was among subjects with middle income (1.6%) with non-significant differences (P= 0.067).

Table (3): Distribution of S. pyogenes concerning parent’s education, job, and monthly income

Variables		F. (%)	GAS		χ²	P- value
Variables		F. (%)	+ve (%)	– ve (%)	χ²	P- value
Father’s job	Employee	153(51)	3(2)	150(98)	1.309	0.457
	Trading	27(9)	1(3.7)	26(96.3)
	Farmer	8(2.7)	0(0)	8(100)
	Other	112(37.3)	1(0.9)	111(99.1)
Mother's job	Employee	42(14)	0(0)	42(100)	0.945	0.342
	Trading	2(0.7)	0(0)	2(100)
	Farmer	3(1.0)	0(0)	3(100)
	Housewife	253(84.3)	5(2)	248(98)
	Other	0	0(0)	0(0)
Education level Father	Illiterate	24(8.0)	0(0)	24(100)	2.727	0.138
	Primary	23(7.7)	0(0)	23(100)
	Intermediate	27(9.0)	0(0)	27(100)
	Secondary	89(29.7)	1(1.1)	88(98.9)
	University	137(45.7)	4(2.9)	133(97.1)
Education level Mother	Illiterate	76(25.3)	2(2.6)	74(97.4)	10.065	0.038
	Primary	46(15.3)	3(6.5)	43(93.5)
	Intermediate	51(17.0)	0(0)	51(100)
	Secondary	83(27.7)	0(0)	83(100)
	University	44(14.7)	0(0)	44(100)
Monthly income	Low	8(2.7)	1(12.5)	7(87.5)	6.560	0.067
	Middle	243(81.0)	4(1.6)	239(98.4)
	Upper	49(16.3)	0(0)	49(100)

Significant statistics at P-value < 0.05. χ² = Chi-square test.

Prevalence of S. pyogenes concerning housing and sharing tools

This data showed that the S. pyogenes carriage was detected among participants who lived in a single house (2.9%), less than 5 individuals lived per room (1.5%), less than 5 children lived in a household (2.3%) with non-significant differences (P > 0.05). Moreover, S. pyogenes carriage was significantly recovered from participants who didn’t share their clothes with others (2.1%), shared their towels (3.6%), and didn’t share their shaving tools (1.5%) with non-significant differences (P > 0.05) (Table 4).

Table (4) Distribution of S. pyogenes concerning housing and sharing tools

Variables		F. (%)	GAS		χ²	P- value
Variables		F. (%)	+ve (%)	–ve (%)	χ²	P- value
Housing	Mixed	266(88.7)	4(1.5)	262(98.5)	0.380	0.539
Housing	Single	34(11.3)	1(2.9)	33(97.1)	0.380	0.539
Number of individuals per room	< 5	277(92.3)	5(1.8)	272(98.2)	0.422	0.517
Number of individuals per room	> 5	23(7.7)	0(0)	23(100)	0.422	0.517
Number of children in household	< 5	133(44.3)	3(2.3)	130(97.7)	0.813	0.609
	> 5	29(9.7)	0(0)	29(100)
	0	138(46.0)	2(1.4)	136(98.6)
Sharing clothes	Yes	67(22.3)	0(0)	67(100)	1.462	0.228
Sharing clothes	No	233(77.7)	5(2.1)	228(97.9)	1.462	0.228
Sharing towels	Yes	56(18.7)	2(3.6)	54(96.4)	1.524	0.218
Sharing towels	No	244(81.3)	3(1.2)	241(98.8)	1.524	0.218
Sharing shaving tools	Yes	8(2.7)	0(0)	8(100)	0.139	0.710
Sharing shaving tools	No	292(97.3)	5(1.7)	287(98.3)	0.139	0.710

Significant statistics at P-value <0.05. χ² = Chi-square test

Prevalence of S. pyogenes concerning some clinical risk factors

The current result showed that all study subjects were given negative respondents for the required risk factor and the rate of S. pyogenes was (1.7%) detected among them as illustrated in Table (5). Also, a high rate of S. pyogenes carriage was found among subjects whose none of their families has an upper respiratory infection (2.1%), infected with skin rash due to sore throat previously (12.5%; P = 0.015), and history of hospitalization (3.2%) (Table 5).

Table (5) Distribution of S. pyogenes carriage concerning clinical risk factors

Variables		F. (%)	GAS		χ²	P- value
			+ve (%)	–ve (%)
Fever	Yes	0(0)	0(0)	0(0)	N.A	N.A
	No	300(100)	5(1.7)	295(98.3)
Cough	Yes	0(0)	0(0)	0(0)	N.A	N.A
	No	300(100)	5(1.7)	295(98.3)
Suffer from heart rheumatism	Yes	0(0)	0(0)	0(0)	N.A	N.A
	No	300(100)	5(1.7)	295(98.3)
Receive treatment for rheumatic heart	Yes	0(0)	0(0)	0(0)	N.A	N.A
	No	300(100)	5(1.7)	295(98.3)
One of your family had an upper respiratory infection	Yes	57(19)	0(0)	57(100)	1.193	0.276
	No	243(81)	5(2.1)	238(97.9)
Infected with skin rash due to sore throat previously	Yes	8(2.7)	1(12.5)	7(87.5)	5.886	0.015
	No	292(97.3)	4(1.4)	288(98.6)
History of hospitalization	Yes	31(10.3)	1(3.2)	30(96.8)	0.513	0.476
	No	269(89.7)	4(1.5)	265(98.5)

Significant statistics at P-value <0.05. χ² = Chi-square test, N.A = Not applicable

To our knowledge, the present study is the first study reporting the carriage rate of S. pyogenes in medical students in Yemen country. Out of 300 medical university students enrolled in this study, 50% in each were males and females, and 92% were between the age of 18–24 years. This finding is similar to previous reports [5, 9]. This result revealed that the overall rate of S. pyogenes carriage among university students was (1.7%). This result is in consonance with previous research by Centor et al. [19] showed that 1.1% of S. pyogenes was recorded among asymptomatic students at the University of Alabama.

However, our findings were in disagreement with the results of a previous study in which the prevalence rate of S. pyogenes carriage among adults was reported at 2–46% in Turkey [8], 9.6% in Philadelphia [9], 15.6% in young adult inhabitants of Wielkopolska, Poland [10], between 11.2 to 34% in India [11], 3.6% among pharmacy students in a university in Cyprus [5], 16.9% in Kabul university [12], and 63% among health community in Australia [20].

The difference in prevalence rate may refer to some factors such as variations in geographical locations, size of the sample, study population, hygienic practices, environmental conditions, socioeconomic status, food consumption, and diagnostic techniques employed by the participants [21–23].

This finding found that the females participating had a higher rate of S. pyogenes carriage (2%) compared with males (1.3%). This report is in disagreement with the results by Noori et al. [12] revealed that the colonization rate of S. pyogenes was higher in males (56.8%) than in females (43.2%). Presumably these difference rates could be factors like the degree of social interaction that females might have more communication with family members than males. Although, in theory, both sex equally affected.

In the present result, the high rate of S. pyogenes carriage was observed among the age group of 25–30 years old (8.3%) and the lower was among 18–24 years (1.1%) with a significant difference (P = 0.008). In a study performed in Poland on 205 healthy adults between 18 and 44 years old, only three (1.5%) adults were reported to carry GAS [10]. Also, Levy et al. [9] reported the asymptomatic carriage rate of GAS as 9.6% among students aged 18–27 years.

However, the highest prevalence of S. pyogenes asymptomatic throat carriage was in the lowest age group (19–21 years) compared to other groups, which shows that throat carriage of this organism decreases with age [12].

The present finding showed that the high rate of S. pyogenes carriage was among medical students whose fathers’ jobs are working in the trading field (3.7%) and whose mothers’ jobs working as housewives (2%). A similar report presented that S. pyogenes isolated from subjects whose mother’s occupation was employed (17.0%) and whose fathers’ occupational status was another kind like daily labor, merchant, and student (14.8%) [24].

The present result showed that a higher rate of S. pyogenes carriage was observed among medical students whose fathers and mothers’ held a university certificate (2.9%) and a primary school certificate (6.5%), respectively. According to another study from Ethiopia, the carrier rate of S. pyogenes was high in children who had illiterate parents (15.8%) [24]. Moreover, higher levels of education are linked to an overall better quality of life, including poor behavioral and physical health problems, lower unemployment rates, and lower rates of incarceration [25].

According to monthly income, the medical university students with a low income in this result had the highest rate of S. pyogenes carriage at 12.5%. It was reported in some reports that low-income countries report high S. pyogenes strain diversity compared with high-income countries. The reason why this is so being not clear [26].

The existing result recorded that the prevalence rate of S. pyogenes carriage was detected among medical students who lived in a single house (2.9%), less than 5 individuals lived per room (1.5%), and less than 5 children lived in a household (2.3%). It was found that children from families with more than eleven members had a four-fold greater chance of carrying GAS than children from families with fewer members [27].

It was found that the number of children in the family was an important risk factor. Students with 1–3 children in the family had a 23-fold higher risk of carrying S. pyogenes than those who (p˂0.05), and those students who had 4–6 children in their family, had a 27-fold higher risk of carrying S. pyogenes in their throat than those didn’t have any children (p˂0.05) [12].

Exposure to asymptomatic persons or cases of S. pyogenes infections can also occur at the household level. Such exposure is high in overcrowded households, as discussed earlier. In addition, limited household resources, such as those for washing and laundry, contribute to an increase in bacterial load on the skin of household members, or objects in the house, resulting in increased transmission. Moreover, sharing bedding and personal items like towels is also a predisposing factor for the transmission of S. pyogenes infections. High numbers of social contacts, a key environmental factor, which is common in schools, hospitals, and other enclosed social places, increase the chances of the transmission of S. pyogenes infections (Avire et al., 2021). [28].

This data showed that the S. pyogenes carriage was recovered from participants who didn’t share their clothes with others (2.1%), shared their towels (3.6%), and didn’t share their shaving tools (1.5%). Also, there were non-significant differences reported between house characterization and S. pyogenes prevalence (P > 0.05).

This finding presented that the high rate of S. pyogenes carriage was found among subjects whose none of their families has an upper respiratory infection (2.1%), infected with skin rash due to sore throat previously (12.5%; P = 0.015), and history of hospitalization (3.2%). Similarly, Mearkle et al. [29] demonstrated an increased risk of S. pyogenes transmission within a household when one family member is positive. Moreover, S. pyogenes infections are commonly spread in schools, nurseries, hospitals, care homes, military camps, and homeless shelters [28]. Also, a study by Barsenga et al. [27] revealed a high rate of GAS among those who had a history of hospitalization (13.5%). Also, children who lived with a family member who had a sore throat were twice as likely to colonize group A Streptococcus (GAS) than children who did not have a primary case or sore throat in their household [27].

Limitations of the study

Since the study was a cross-sectional study performed over a short period, the impact of seasonal factors on differences in prevalence could not be determined. The low numbers obtained from the study made statistical analysis challenging. In addition, this study was unable to perform ASO titer and antibiotics susceptibility tests due to a lack of resources.

There was a relatively low rate of S. pyogenes throat carriage in healthy medical students compared with international investigations. This result provides useful baseline data on the GAS carriage rate among healthy adult students in this study area. Therefore, adequate hand and respiratory hygiene and avoiding overcrowded settings should continue to be emphasized as important protective measures for acquiescing infection. Further investigation is needed to understand the epidemiology of S. pyogenes among healthy individuals and associated risk factors other than university students and develop strengthen control and preventive strategies.

Conflict of Interest

The authors declare that they have no competing interests.

Funding Information

Authors received no financial support

Acknowledgment

The authors would like to thank team workers Ali Latef, Muaadh Gaber, Mohammed Bawazir, Saeed Alamodi, Omer Al-Aidaros for specimens collection, isolated and identified the bacteria. Also, we thank Dr. Gader Hasan, Dr. Lamis Al-Ghouli, Dr. Tammam Al-Saqqaf, and Dr. Ahmed Al-Ruwaisi and all members of staff of the medical laboratories at Queen Arwa University for their help in specimen analysis.

Author’s Contribution

Nasser Al-Aomary and Lutf Alrahabi conceived and designed the experimental study. Nasser Al-Aomary isolated and identified the bacteria. Wadhah Edrees and Bashir Al-Ofairi analyzed and presented the results in figures and tables. Also, Wadhah Edrees and Nasser Al-Aomary prepared and wrote the manuscript. All authors reviewed, revised, and approved the manuscript for submission.

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The Rate of Asymptomatic Throat Carriage of Streptococcus pyogenes and its Associated Risk Factors among Medical Students of Queen Arwa University in Sana’a City, Yemen

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Abstract

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Introduction

Materials and Methods

Study area and period

Study population

Sample size

Information collection

Inclusion and exclusion criteria

Specimen size and collection

Ethical considerations

Statistical analysis

Results

Discussion

Limitations of the study

Conclusion

Declarations

References

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