Microbial Bowel Infections-Induced Biochemical and Biological Abnormalities among Young Egyptian Swimmers: Associated Risk Factors Affecting Swimming Performance Running title: Swimmers’ Microbial Bowel Infections and Swimming Performance

doi:10.21203/rs.3.rs-2113868/v1

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Microbial Bowel Infections-Induced Biochemical and Biological Abnormalities among Young Egyptian Swimmers: Associated Risk Factors Affecting Swimming Performance Running title: Swimmers’ Microbial Bowel Infections and Swimming Performance

https://doi.org/10.21203/rs.3.rs-2113868/v1

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published 21 Mar, 2023

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Swimmers’ personal hygiene affects the spread of microbes in swimming pools. The present study aimed to determine the incidence of microbial infections among young Egyptian swimmers and its impact on biochemical parameters, and swimming performance. From January 2020 to June 2021, 528 public club swimmers were examined cross-sectionally. Swimmers were divided into two groups according their scores in the competition (group1 with high score and group 2 with low score). Stool samples, biochemical parameters and complete blood picture were assessed. Biological measures were evaluated directly after swimming. Microbial infections were 54% for intestinal parasitosis, 2.8% for H. pylori. Blastocystis spp. and Cryptosporidium spp. infected 24.1% and 23.3% of swimmers, respectively. Infection rates among swimmers’ groups varied according to gender, age, swimming duration and frequency. Infected swimmers with cryptosporidiosis had higher ALT, WBCs, and differential cells but lower AST levels. The results revealed high prevalence of Blastocystis spp., Cryptosporidium spp., and microsporidia. Swimming habits, frequency, and duration influenced the infectious status that induced anemia, abnormal blood pressure and heart rate. Giardiasis, showed reduction in the biochemical markers including ferritin, lactoferrin, iron and transferrin among group2 as compared to group1. Thus, raising swimmers’ hygiene awareness and targeting health education is obliged.

intestinal parasitic infections

microbial bowel infection

swimming habits

anemia

abnormal blood pressure

biochemical parameters.

Water-borne infections are a serious public health concern with a global impact, as it causes more than 2.2 million deaths per year¹. Swimming pools are of special concern because of their warm and moist environment, which allows pathogenic organisms to thrive. Pools pose a significant public health hazard because of the large number of potential pathogens and transmission routes². Swimming pools are contaminated with pathogens associated with swimmers, such as vomit, saliva, mucus, and perspiration, causing respiratory, dermal, and central nervous system disorders³. Swallowing recreational water infects swimmers, leading to outbreaks in both developing and developed countries⁴. If the pools had been well-managed and the awareness of swimmers’ hygiene had been raised, several outbreaks related to swimming pools can be avoided.

Although swimming offers a variety of advantages including physical activity, socialization, and competition, it can lead to a variety of infectious diseases⁵. Physical contact among athletes and the sharing of equipment, such as wearing personal protective equipment or braces, towels, showers, and locker rooms, could result in the transmission of infections⁶.

Athletes are at risk of intestinal parasitic infections (IPIs) because of poor environmental conditions in sports situations. Athletes are exposed to inadequate food and environmental hygienic conditions during preparation camps, national team camps, and frequent travel⁷. In addition, competition stress may render athletes temporarily more vulnerable to infectious illness⁸. Athletes who engage in long-term and strenuous exercise frequently have their immune systems suppressed⁹. Heavy exercise increases the risk of illness by allowing microorganisms to enter the body¹⁰. As a result, athletic performance may be impaired and the severity of the disease process could be augmented^8,11.

Parasitic infections may result in several alterations in host biomarkers, such as ferritin, transferrin, iron, and lactoferrin contributing to the swimmers’ performance. There is a scarcity of data regarding the changes in the biochemical parameters induced by each parasite¹². IPIs may cause anemia in athletes and adversely affect their performance. This may cause low Hb concentration during anemia, which is mostly induced by iron deficiency. In turn, reduced iron content negatively affects aerobic capacity, muscle strength, and endurance^13,14.

Regular exercise is well acknowledged as a first-line approach for preventing blood pressure (BP) rises¹⁵. Endurance training, such as swimming, alters traditional markers of physical fitness in athletes, along with changes in various cardiovascular parameters, including a heart rate (HR) reduction¹⁶. HR variability in athletes has been recognized as a useful tool for examining long-term changes associated with exercise and autonomic nervous system activity during exercise¹⁷, as well as fitness and performance monitoring¹⁸. However, studies on the influence of swimming on HR and its value in professional application are still rare.

Water-borne disease monitoring and analysis are critical for prevention and control. Due to the scarcity of scientific literature on this subject and the popularity and potential benefits of swimming, the aim of the current study was to investigate the prevalence of microbial bowel infections and its relevance to biochemical and biological parameters affecting swimming performance among young swimmers.

Study design and population

A cross-sectional study was conducted from January 2020 to June 2021, to determine the prevalence of IPIs, H. pylori, and related risk factors among young swimmers in a public swimming pool in Alexandria, Egypt. The study population was composed of young swimmers, aged from 5 to 18 years old. The total number of participants was 528 (339 males and 189 females). The swimmers were divided into two groups who achieved a high score (Gp1) according to the time spent in the Winter Alexandria Championship 2020 for swimmers aged 12 years old. In which boys and girls swam 100 LC Meter Freestyle and the best record for boys was 59.17, and that for girls was 1:02.02. Meanwhile, Gp2 included swimmers who had low records, and who were still being trained. An informed consent was obtained from parents of the young swimmers after explaining the purpose of the study and before collecting demographic data, blood, and stool samples. The name of the participants is remained confidential. No one will have access to his/her medical file except for the research physician and his assistants, independent professional ethics committees, and inspectors from regulated government departments. The study was approved by the ethics committee of the Faculty of Pharmacy, Pharos University in Alexandria. (PUA01202012103017). All methods were performed in accordance with the Declaration of Helsinki.

Sample collection and processing

A structured questionnaire based on known risk factors was developed. The participants in the study (the parents in the case of younger swimmers) were interviewed to collect socio-demographic data, as well as, information on behavioral and hygienic practices. Two fresh stool samples were collected on two alternative days from each participant. Fresh samples were subjected to H. pylori Ag detection, and then 4 thin smears were prepared after air drying. Two slides of them were stained by trichrome, and the others by quick hot Gram chromotrope for detecting microsporidia spp. according to standard procedures^19,20. Another portion from each stool sample was preserved in formol saline (5%) to be later concentrated using the formol-ethyl acetate sedimentation technique, and then two permanently stained smears were prepared from the sediment, fixed, and stained with the MZN technique according to standard procedures²¹. Concerning blood samples, 528 serum samples were collected for assessing some biochemical parameters including ferritin, transferrin, iron, lactoferrin, and liver enzymes (ALT and AST) and only 291 EDTA-blood samples were collected for determining a complete blood picture. In addition, some biological measures such as blood pressure and heart rate were measured directly at the end of the swimming session.

Kits:

In the present study, the biomarker ferritin was determined by Human FTH (Ferritin, Heavy Polypeptide) ELISA Kit, Elabscience (Catalog Number: E-EL-H2010). Transferrin was estimated by Biosystem kit (Cod: 130910); iron was measured by Biosystem kit (COD 11554); and lactoferrin was estimated by Thermo Fisher Human LTF/Lactoferrin ELISA Kit (Cat.No.: EH309RB).

Statistical analysis:

Data were entered, verified, and analyzed using SPSS v.25.0 (IBM, Armonk, USA). Differences and associations were tested using Pearson's chi-squared or Fisher's exact test, the mean calculated by Mann-Whitney, and the odds ratio (OR) with its corresponding 95% confidence interval (CI) was calculated to identify the possible predictors of infection or association as shown in Table 1.

Table 1

Interpretation of the odds ratio²²:
OR < 1	95% CI	Interpretation
0.71	0.68–0.84	Significant protective value
0.71	0.42–1.06	Possible protective value but not Significant
OR > 1	95% CI	Interpretation
1.21	1.07–1.56	Significant risk factor
1.21	0.72–1.69	Possible risk factor but not Significant
OR = 1	95% CI	Interpretation
1.00	1.00–1.00	No effect, or no association

Table 2 shows that males were more likely than females to undertake the study (64.2% vs. 35.8%). Swimmers under ten years were fewer than swimmers who were older than ten years (43.2% vs. 56.8%). Swimmers who practiced swimming for less than five years and those who practiced for ≥ 5 years recorded similar rates (51.1% vs. 48.9%). The percentage of swimmers who swam < 4 days/week was higher than those who swam ≥ 4 days/week (63.1% vs. 36.9%).

Table 2

Distribution of young swimmers according to some demographic and swimming data, some clinical manifestation, and some physiological and hematological parameters.
Demographic data		Swimmers (N = 528)
Demographic data		No.	%
Gender
	Male	339	64.2
	Female	189	35.8
Age (years)
	≤ 10	228	43.2
	> 10	300	56.8
Swimming data:
Duration of swimming (years)
	< 5	270	51.1
	≥ 5	258	48.9
Frequency of Swimming (day/week)
	< 4	333	63.1
	≥ 4	195	36.9
Alexandria Championship Scores
	Gp1	90	17.0
	Gp2	438	83.0
Clinical manifestations:
Non-GI Symptoms
Skin rash		51	9.7
Eye allergy		24	4.5
Chest allergy		24	4.5
Otalgia		9	1.7
Allergic Rhinitis		141	26.7
Fever		36	6.8
Headache		63	11.9
GI-Symptoms:
Diarrhea		72	13.6
Nausea		33	6.3
Constipation		93	17.6
Abdominal colic		222	42.1
Anal itching		18	3.4
Dysentery		18	3.4
Stomachache		27	5.1
Some physical and physiological parameters
Heart rate:
*Abnormal		45	8.5
*Normal		483	91.5
Blood Pressure:
*Abnormal		114	21.6
*Normal		414	78.4
Hemoglobin: (N = 291)
*Anemic		27	9.3
*Normal		264	90.7
Gp1: Swimmers who achieved the best records (Boy: 59.17, Girl: 1:02.02)
Gp2: Swimmers who achieved low records & under training

The rate of swimmers who spent a shorter time in the championship was lower than among those who spent a longer time (17% vs. 83%). Regarding the clinical characteristics of swimmers, rhinitis was the most frequent of the non-GIT symptoms (26.7%), followed by headache, skin rash, and fever (11.9%, 9.7%, and 6.8%, respectively), then by eye allergy, chest allergy, and otalgia (4.5%, 4.5%, and 1.7%, respectively). Concerning GIT symptoms, abdominal colic showed the highest rate (42.1%), followed by constipation and diarrhea (17.6% and 13.6%, respectively), then nausea, stomachache, and equal rates of anal itching and dysentery) (6.3%, 5.1%, and 3.4%, respectively). As for biological measures, the rates of swimmers who showed abnormal HR, abnormal BP, and anemia were 8.5%, 21.6%, and 9.3%, respectively.

Table 3 shows that the rate of IPIs was 54%, and the total microbial infection was 54.5%. The highest rates of microbial infections were Blastocystis spp. and Cryptosporidium spp. (24.1% and 23.3%, respectively), followed by G. lamblia and E. histolytica (14.2%, and 12.7%, respectively). In contrast, Cyclospora, H. pylori, Microsporidia spp., I. belli, D. fragilis, E. coli, and A. lumbricoides were present at lower rates (5.7%, 2.8%, 2.5%, 1.7%, 1.1%, 1.1%, and 0.9%, respectively). Concerning Gp1 and Gp2 in that table, Gp2 showed statistically significant differences in IPI & microbial infection as compared to Gp1. Approximately B. hominis showed an equal rate of infection among both groups. The rate of each parasite among Gp2 was higher than Gp1. Only the infected swimmers with giardiasis showed a statistically significant difference. In contrast, although H. pylori showed a high rate of infection among Gp1 as compared to Gp2, there was no statistically significant difference observed.

Table 3

Distribution of the microbial infections among young swimmers and their effect on the time of competition in the Winter Alexandria Championship 2020:
Microbial Infections	No. +ve		Gp 1 No. examined = 90		Gp 2 No. examined = 438		P-value
Microbial Infections	No.	%	No. +ve	%	No. +ve	%	P-value
B. hominis	127	24.1	22	24.4	105	24.0	0.924
Cryptosporidium	123	23.3	16	17.8	107	24.4	0.218
Cyclospora	30	5.7	3	3.3	27	6.2	0.452
I.belli	9	1.7	0	0.0	9	2.1	0.369
Microsporidia	13	2.5	0	0.0	13	3.0	0.139
G. lamblia	75	14.2	6	6.7	69	15.8	0.030*
E. histolytica	67	12.7	10	11.1	57	13.0	0.729
Dientameba fragilis	6	1.1	0	0.0	6	1.4	0.596
E. coli	6	1.1	0	0.0	6	1.4	0.596
Ascaris lumbricoides	5	0.9	0	0.0	5	1.1	0.308
Total IPI	285	54.0	34	37.8	251	57.3	0.001*
H. pylori	15	2.8	3	3.3	12	2.7	0.729
Total microbial infections	288	54.5	37	41.1	251	57.3	0.005*
*: Statistically significant at p ≤ 0.05

Table 4 shows that the rate of IPI among males and females in Gp2 was higher than in Gp1 (57.2% vs. 37.3% and 57.5% vs. 40%, respectively). Moreover, females showed a significant risk of IPI (3.3-fold) as compared to males (P < 0.001). Gp 2 showed higher rates of IPI compared with Gp1 58.2% vs. 0.0% respectively, among swimmers aged ≤ 10 years; and 56.3% vs. 39.1% respectively, among swimmers aged > 10 years, with a significantly higher risk of IPI (30.6-fold) among swimmers aged up to 10 years compared with those older than ten years (P < 0.001). As for the duration of swimming, Gp1 showed a slightly higher rate of infection as compared to Gp2 swimmers who practiced swimming for < 5 years (55.6% vs. 53.9%). In contrast, Gp2 showed a higher rate of infection compared with Gp1 among those who practiced swimming for ≥ 5 years (61.5% vs. 30.2%), with the former exhibiting a significantly higher (3-fold) risk compared with the latter (P < 0.001). Regarding the frequency of swimming, the rate of infection among Gp2 was higher than Gp1 who swam < 4 days/week (56.9% vs. 44.4%). Similarly, those who swam ≥ 4 days/week showed a clear difference (58.3% vs. 34.9%). Moreover, the former group had a significantly higher (5-fold) risk compared with the latter (P < 0.001).

Table 4

Intestinal parasitic infections in relation to some demographic and swimming data, physiological, hematological parameters, and biomarkers of young swimmers, and their effect on swimmers’ performance in the Winter Alexandria Championship 2020
Parameters	IPI						OR	P-value	Total
	Gp 1			Gp 2					Total
	Total examined		No. +ve (%)	Total examined		No. +ve (%)			Examined		Infected N(%)
Gender
Male	75		28 (37.3)	264		151 (57.2)	1.000	< 0.001^*	339		179(52.8)
Female	15		6 (40)	174		100 (57.5)	3.295 (1.833–5.924)	< 0.001^*	189		106(56.1)
Age
≤ 10	3		0 (0.0)	225		131 (58.2)	30.634 (9.545–98.316)	< 0.001^*	228		131(57.5)
> 10	87		34 (39.1)	213		120 (56.3)	1.000	< 0.001^*	300		154(51.3)
Duration of Swimming (in years)
< 5 years	27		15 (55.6)	243		131 (53.9)	2.908 (1.784–4.740)	< 0.001^*	270		146(54.1)
≥ 5 years	63		19 (30.2)	195		120 (61.5)	1.000	< 0.001^*	258		139(53.9)
Frequency of swimming (days/week)
< 4days/week	27		12 (44.4)	306		174 (56.9)	5.409 (3.298–8.873)	< 0.001^*	333		186(55.9)
≥ 4days/week	63		22 (34.9)	132		77 (58.3)	1.000	< 0.001^*	195		99(50.8)
Blood Pressure
Normal	75		28 (37.3)	339		201 (59.3)	1.000	0.215	414		229(55.3)
Abnormal	15		6 (40.0)	99		50 (50.1)	1.460 (0.803–2.655)	0.215	114		56(57.0)
Heart rate
Normal	87		31 (35.6)	396		222 (56.1)	1.000	0.065	483		253(52.4)
Abnormal	3		3 (100)	42		29 (69.0)	3.076 (0.932–10.152)	0.065	45		32 (71.1)
Hemoglobin**
Normal	69		31 (44.9)	195		105 (53.8)	1.000	0.098	264		136 (51.5)
Abnormal	3		0 (0.0)	24		21 (87.5)	2.831 (0.826–9.697)	0.098	27		21 (77.8)
Biochemical Markers (Mean ± S.E.)
Ferritin ng/ml	34	106.5 ± 9.45		251	83.82 ± 3.65		0.991 (0.987–0.996)	< 0.001^*	285	86.53 ± 3.43
Transferrin mg/dL	34	306.1 ± 5.54		251	297.5 ± 2.63		0.992 (0.985–0.998)	0.017^*	285	298.5 ± 2.41
Iron µg/mL	34	115.7 ± 5.73		251	103.6 ± 2.67		0.993 (0.986–0.999)	0.022^*	285	105.1 ± 2.46
Lactoferrin ng/mL	34	372.6 ± 15.26		251	365.3 ± 6.26		0.997 (0.995–0.999)	0.015^*	285	366.1 ± 5.80
ALT	34	21.68 ± 1.48		251	21.28 ± 0.47		1.010 (0.981–1.040)	0.520	285	21.33 ± 0.45
AST	34	28.56 ± 1.74		251	27.38 ± 0.57		0.999 (0.974–1.023)	0.912	285	27.52 ± 0.54
OR: Odds ratio CI: Confidence interval LL: Lower limit UL: Upper Limit
: Statistically significant at p ≤ 0.05 *: sample size was 291
Gp1: Achieved the best record in the Championship
Gp2: The swimmers who have a long time in the Championship or who are under training
N.V. of Hb: 11.5 g/dl for children aged 5–10 years and 12.0 g/dl for children aged 10–18 years

Concerning BP, the rates of IPI among Gp2 were higher than Gp1 for both normal BP and abnormal BP (59.3%vs.37.3%, and 50.1% vs. 40.1%, respectively). Swimmers with abnormal BP exhibit a higher IPI rates (1.5-fold) than those with normal BP. Also, swimmers with abnormal heart rates showed higher IPI rates (3.076-fold) than swimmers with normal HR. Similarly, anemic swimmers showed a higher IPI rates (2.831-fold) than normal ones.

In table (4), Gp2 showed a statistically significant reduction in the biomarkers as compared to Gp1. This included ferritin (83.82 ± 3.65 vs. 106.5 ± 9.45), transferrin (297.5 ± 2.63 vs. 306.1 ± 5.54), iron (103.6 ± 2.67 vs. 115.7 ± 5.73), and lactoferrin (365.3 ± 6.26 vs. 372.6 ± 15.26), while the O.R. showed significant protective values. But no statistically significant difference was found, although ALT was higher among Gp2 compared to Gp1 (22.0 ± 0.38 vs. 21.4 ± 0.84). Inversely, AST was higher among Gp1 as compared to Gp2 (27.9 ± 1.01 vs. 27.8 ± 0.44).

In table (5), swimmers infected with giardiasis showed a statistically significant reduction in the mean of ferritin, transferrin, iron, and lactoferrin as compared with non-infected ones [(21.7 vs. 110.7), (264.4 vs. 312.3), (54.5 vs. 121.5), and (288.8 vs 394.9) respectively]. The same was found among infected Gp1 with giardiasis except in transferrin but with no a statistically significant difference [(44.5 vs. 123.8), (287.8 vs. 315.7), (65.7 vs. 124.1), and (304.3 vs. 409.1) respectively]. In total giardiasis, infected GP2 showed a statistically significant reduction in ferritin, transferrin, iron, and lactoferrin as compared with non-infected ones [(19.7 vs 107.8), (262.4 vs 311.5), (53.6 vs 120.9), and (287.5 vs 391.7) respectively].

Table (5): Giardia lamblia in relation to some biomarkers and their effects on swimmers’ performance:

Biomarkers	Total Examined (n = 528)		P₀	Gp1 (n = 90)		P₀	Gp2 (n = 438)		P₀	P between + ve Gp1 & Gp2
Biomarkers	-ve (n = 453)	+ve (n = 75)	P₀	-ve (n = 84)	+ve (n = 6)	P₀	-ve (n = 369)	+ve (n = 69)	P₀	P between + ve Gp1 & Gp2
Ferritin	110.7	21.7	< 0.001^*	123.8	44.5	< 0.001^*	107.8	19.7	< 0.001^*	0.005^*
Transferrin	312.3	264.4	< 0.001^*	315.7	287.8	0.082	311.5	262.4	< 0.001^*	0.274
Iron	121.5	54.5	< 0.001^*	124.1	65.7	< 0.001^*	120.9	53.6	< 0.001^*	0.178
Lactoferrin	394.9	288.8	< 0.001^*	409.1	304.3	0.002^*	391.7	287.5	< 0.001^*	0.407
Data were expressed using Mean
p₀: p-value for Mann-Whitney test for comparing Negative and Positive
p: p-value for Mann-Whitney test for comparing Positive cases of Gp1and Gp2
*: Statistically significant at p ≤ 0.05

In table (6), infected swimmers with cryptosporidiosis recorded a higher ALT level and a lower rate of AST as compared with non-infected ones [(22.08 vs. 21.35) and (26.98 vs. 28.07) respectively] with no statistically significant differences. Similarly, infected Gp1 and Gp2 showed a higher ALT level and a lower rate of AST as compared with non-infected ones [(21.81 vs. 19.62) and (26.38 vs. 28.24) respectively] and [(22.14 vs. 21.61) and (27.07 vs. 28.03) respectively] respectively. Concerning the hematological parameters among swimmers infected with cryptosporidiosis, there is a statistically significant difference in the reduction of RBCs mean among infected swimmers, but there is no statistically significant difference among infected Gp1, and Gp2 as compared with non-infected ones [(4.69 vs. 4.83), (4.7 vs. 5.19), and (4.68 vs. 4.75) respectively]. In contrast, Hb conducted increased rates among infected swimmers, infected Gp1, and infected Gp2 as compared to non-infected ones [(14.0 vs. 12.82), (12.95 vs. 12.34), and (14.25 vs. 12.79) respectively]. There are statistically significant differences in both Gp1 and Gp2. Also, there is an increase in the HCT among infected swimmers, Gp1, and Gp2 as compared to non-infected ones [(38.63 vs. 38.52), (38.97 vs. 37.23), and (38.95 vs. 38.35) respectively], but there are no statistically significant differences.

Table (6): Cryptosporidium spp. in relation to some biomarkers and their effects on swimmers’ performance:

Biomarkers	Total Examined (n = 528)		P₀	Gp1 (n = 90)		P₀	Gp2 (n = 438)		P₀	P between + ve Gp1 & Gp2
Biomarkers	-ve (n = 453)	+ve (n = 123)	P₀	-ve (n = 74)	+ve (n = 16)	P₀	-ve (n = 331)	+ve (n = 107)	P₀	P between + ve Gp1 & Gp2
ALT	21.35	22.08	0.840	19.62	21.81	0.575	21.61	22.14	0.967	0.366
AST	28.07	26.98	0.309	28.24	26.38	0.519	28.03	27.07	0.405	0.830
RBC**	4.83	4.69	0.043^*	5.19	4.70	0.467	4.75	4.68	0.076	0.436
Hb**	12.82	14.0	0.380	12.34	12.95	0.001^*	12.79	14.25	0.055	0.002^*
HCT**	38.52	38.63	0.720	37.23	38.97	0.118	38.35	38.95	0.172	0.149
WBC**	6.68	6.76	0.657	6.50	7.04	0.345	6.55	6.82	0.600	0.427
N**	43.80	48.84	0.002^*	45.35	45.61	0.860	43.12	49.64	< 0.001^*	0.922
L**	41.28	45.56	0.008^*	42.94	43.53	0.676	40.90	46.33	0.002^*	0.774
M**	6.28	6.44	0.814	5.92	6.18	0.446	6.38	6.53	0.902	0.446
E**	2.38	3.01	0.551	2.88	3.76	0.945	2.25	2.73	0.594	0.489
B**	0.57	0.80	0.093	0.69	0.80	0.679	0.51	0.83	0.032^*	0.103
Data were expressed using Mean
p₀: p-value for Mann-Whitney test for comparing Negative and Positive
p: p-value for Mann-Whitney test for comparing Positive cases of Gp1and Gp2
: Statistically significant at p ≤ 0.05 *: sample size was 291

Table (6) shows that there is an increase in the mean of the total white blood cells (6.76 vs. 6.68), neutrophils (48.84 vs. 43.8), lymphocytes (45.56 vs. 41.28), monocytes (6.44 vs. 6.28), eosinophils (3.01 vs. 2.38), and basophils (0.8 vs. 0.57) among infected swimmers with cryptosporidiosis as compared with non-infected ones with no statistically significant differences except in N and L. Also, the means of WBCs, N, L, M, E, and B among infected Gp1 (7.04, 45.61, 43.53, 6.18, 3.76, and 0.8, respectively) are higher than the noninfected ones with no statistically significant differences (6.5, 45.35, 42.94, 5.92, 2.88, and 0.69, respectively). These means are high among infected Gp2 as compared with non-infected ones with statistically significant differences in N, L, and B [(6.82 vs. 6.55), (49.64 vs. 43.12), (46.33 vs. 40.90), (6.53 vs. 6.38), (2.73 vs. 2.25), and (0.83 vs. 0.51) respectively].

The current study, rhinitis showed the highest rate of non-gastrointestinal symptoms followed by headache, skin rash, and fever (11.9%, 9.7%, and 6.8%, respectively). Which stem from the pathogens brought into the pool by infected swimmers or by inadequate hygiene². Meanwhile, eye and chest allergy, and otalgia (4.5%, 4.0%, and 1.7% respectively), showed the lower rates. However, the most common GI symptoms reported were abdominal colic (28.4%), constipation (17.6%), diarrhea, and abdominal discomfort (13.6%), followed by nausea (6.3%), stomachache (5.1%), and anal itching and dysentery (3.4% each). Some other studies found similar results. Hlavsa et al.²³, reported that gastroenteritis was the most prevalent waterborne disease, followed by infections of the upper respiratory tract, skin, eye, and nasal cavity. In addition, a previous study found outbreaks of GI symptoms linked to the use of disinfected recreational water as swimming pools²⁴. Illness from exposure to recreational water exposure is common. Infield studies of swimmer illness diarrhea rates of 3% − 8% were found in follow-up health surveys²⁵. It was reported that 10,000 cases of diarrheal illness were associated with 32 recreational water-borne disorders outbreaks associated with disinfected water. This number was probably higher because diarrheal illness is underreported to the public health authorities^24,26. Sanborn and Takaro²⁷ reported that there is a 3% − 8% risk of acute GI illness (AGI) after swimming. Children aged < 5 years, the elderly, and immunocompromised patients are vulnerable groups for AGI. Children are at a higher risk because they swallow more water when swimming.

Concurrent infection with single or multiple parasites was observed among the study participants. The predominant microbes detected were Blastocystis spp., Cryptosporidium spp., G. lamblia, and E. histolytica (24.1%, 23.3%, 14.2%, and 12.7%, respectively). Other less common infections were also detected, including Cyclospora, H. pylori, microsporidia spp., I.belli, D. fragilis, E. coli, and A. lumbricoides infections (5.7%, 2.8%, 2.5%, 1.7%, 1.1%, 1.1%, and 0.9%, respectively). Soller et al.²⁸ reported that Giardia spp. is found in swimming water at much higher concentrations. In 2003–2004, it was revealed that Cryptosporidium spp. 55.6% and Giardia spp. 5.6% were responsible for gastroenteritis outbreaks related to swimming pools in the US²⁹. The majority of AGI outbreaks in swimming pools recorded during the peak swimming season (32 out of 34) between 2011 and 2012 were related to Cryptosporidium spp. Moreover, cryptosporidiosis incidence in the U.S. is doubled in children compared with adults, and infections predominantly occur following exposures to pool water contaminated with Cryptosporidium shed by infected swimmers³⁰. According to the annual report of the British Columbia Centre for Disease Control, cryptosporidiosis incidence increased to 1.6 instances per 100,000 people in 2012, whereas giardiasis cases remained steady at 13.3/100,000 population³¹. The greater infection rates detected in young children may be attributed to the fact that their immune systems are underdeveloped, and they ingest more pool water than do adults do³².

Despite being important and popular, swimming pools pose some public health risks to swimmers because of microbiological contamination³³. Swimming involves sharing water with many other persons in a pool; consequently, the water contains various bodily fluids, dirt, and debris that wash off bodies during swimming activities³⁴. Although chlorine is an effective disinfectant, it does not kill all pathogens³⁵. Some pathogens, such as Cryptosporidium spp., are highly resistant to the chlorine concentrations routinely used in pools³⁶. Causes of microbiological contamination of swimming pools include irregular chlorination, deficiency infiltration, and high load swimmers. In addition, the sanitary condition of swimmers would be more difficult to control³⁷.

Improvements in swimmer's health require changes in knowledge, attitude, and behavior. Therefore, interventions based on social and behavioral science theories are necessary. Implementation of a public health education program for swimmers is essential³⁸. The large number of young swimmers exposed to IPIs from pool water in this study provides a strong incentive to review the factors associated with IPI transmission and improve the recommendations to reduce the transmission of gastrointestinal disease caused by swimming pools. These recommendations are meant to eliminate infectious disease transmission by advising swimmers to avoid pool water swallowing and refraining from swimming when experiencing diarrhea. Showering before and during swimming, as well as regular bathroom breaks should be promoted among young children³⁹.

Epidemiological studies of the prevalence of IPIs in different localities have a primary goal of identifying high-risk factors related to communities and designing appropriate interventions⁴⁰. In line with this view, the current study attempted to assess the prevalence of different IPIs and the associated risk factors among young swimmers in a public swimming pool in Alexandria, Egypt. The findings of this study revealed a particularly high prevalence of several intestinal parasites with public health implications among young swimmers. Several factors, including swimming duration, frequency, BP, HR, and anemia, were found to be linked to IPIs in young swimmers. These infections put swimmers at risk of developing morbidities. In addition, swimmers may be a source of infection for the wider community. Therefore, there is a need for their consideration in ongoing interventions by placing special emphasis on the identified factors, to meet national and international goals for eliminating these infections as a public health concern should be considered.

The current findings demonstrated that the female study participants had a higher risk of having IPIs than did males as illustrated by the prevalence of IPIs among young male and female swimmers. Regarding the age of the participants, a higher risk of IPIs was found to be among swimmers aged up to 10 years compared with those who were older than 10 years old. This may be attributed to the fact that older swimmers are usually more familiar with the importance of hygiene and comply with swimming-related health education than younger swimmers. Heaney et al⁴¹. reported that children aged < 10 years of age contract more illness from recreational water because they stay in the water longer, have hand-to-mouth exposure, immerse their heads more often, and swallow more water while swimming.

The duration of swimming was one of the parameters that were significantly associated with parasitic infection. According to the current study, it was shown that the rate of infection among swimmers who practiced swimming for < 5 years was higher than that detected among those who practiced swimming for ≥ 5 years in group 1, whereas in group 2, higher infection rates were observed among swimmers who practiced swimming for ≥ 5 years vs. those who practiced swimming for < 5 years. This can be partially explained by the frequent suppression of the immune system in athletes who perform long-term and heavy exercises, which renders making them more susceptible to infections^9,10, and results in poor performance^11,42.

The rate of infection among swimmers who practiced swimming less frequently in the current study (less than 4 days/week) was 5-fold higher than that observed among swimmers who practiced swimming 4 days or more per week. In contrast, a previous study reported that swimming frequency does not appear to affect swimmers², and consequently does not affect the infection rate among swimmers.

The current findings demonstrated that abnormal BP was among the hazards of IPIs. Leitch and He revealed that Cryptosporidium infection appeared to be associated with hypotension among the participants, this could be partially explained by the fact that immunity plays a critical role in guarding against Cryptosporidium infection and in parasite elimination⁴³. As previously documented in several studies, intense exercise that occurs during competition causes immunosuppression⁴⁴, which is responsible for hypotension⁴⁵. Moreover, moderate exercise activates the immune system against diseases⁴⁴, with T cells playing a significant role in the induction of hypertension⁴⁶. This might explain hypertension observed among some swimmers in this study.

A significant interaction between the autonomic and the immune systems plays a critical role in the initiation and maintenance of hypertension and results in cardiovascular diseases, end-organ damage, and mortality. In addition, a consistent association exists between hypertension, proinflammatory cytokines, and cells of the immune system⁴⁷.

Regarding heart rate, swimmers with an abnormal HR showed higher rates of being infected compared with a normal HR. During exercise, substantial cardiovascular adjustments occur to meet the competing metabolic demands of the working muscles and the thermoregulatory demands of the skin blood flow⁴⁸. Exercise, particularly endurance training, is associated with increases in parasympathetic activity at rest⁴⁹, resulting in a decreased HR which could explain the bradycardia observed among the current study participants.

Changes in cardiac autonomic activity and/or alterations of electrophysiology of the pacemaker cells have been previously reported to be among the mechanisms that explain the resulting relative bradycardia^16,50. The effects of training on HR autonomic regulation have also been previously investigated in the recovery phase at the end of the exercise, where a faster kinetic of HR decay has been shown to occur as a consequence of training⁵¹.

Anemia is commonly caused by IPIs in athletes and is associated with iron deficiency, loss of weight, and diarrhea among children^13,14. Intestinal parasites, which were asymptomatic, do not cause iron-deficiency anemia in athletes. Symptoms might occur at the time of weakening of the immune system. Intestinal parasites are resistant to elimination from the host because of the weak natural immunity against these parasites. Consequently, most intestinal parasites are chronic as they can adapt to the host's natural defense mechanisms and continue to multiply⁵².

In the present study, infected swimmers with giardiasis showed a statistically significant reduction in the mean of ferritin, transferrin, iron, and lactoferrin as compared with non-infected ones [(21.7 vs. 110.7), (264.4 vs. 312.3), (54.5 vs. 121.5), and (288.8 vs 394.9) respectively]. That was consistence with that reported by Al-Hadraawy et al., that recorded a significant decrease in ferritin and iron among infected patients who have meant the laboratory of AL-Hakeem hospital and AL-Zahra maternity and pediatrics in AL-Najaf province. Ferritin was [(14.91 ± 1.997) and (20.55 ± 3.6) among males and females respectively] compared with the control group [(185.7 ± 52.25) and (180.6 ± 43.09) respectively], and iron was [(42.18 ± 4.802) and (44.19 ± 8.352) respectively] compared with the control group [(206.5 ± 8.918) and (164.8 ± 38.58) respectively]⁵³. A year later, Abood⁵⁴ recorded a significant decrease in serum lactoferrin, ferritin, and iron concentration of patients with G. lamblia infection [(14.83 ± 0.301),(124.873 ± 0.064) and (44.631 ± 0,083) respectively] compared to the control group [(20.34 ± 0.412),(326.312 ± 0.132) and (131.82 ± 0.710) respectively]. Also, it agrees with other studies done among children suffering from giardiasis^55,56. That was attributed to the high load of giardiasis which lead to iron malabsorption^57,58. The present study attributed the low record of infected Gp2 in the competition to the reduction in the biomarkers among them as compared to infected Gp1 [(19.7 vs. 44.5), (262.4 vs. 287.8), (120.9 vs. 65.7), and (287.5 vs. 304.3), respectively]. That was consistent with that reported by Damian⁵⁹ who observed that insufficient reserves of iron in the body can reduce athletic performance, which may be manifested as fatigue, exercise intolerance, or even cognitive function impairment.

The present findings showed that there was an increase in the mean of the total WBCs, N, L, M, E, and B among infected swimmers with cryptosporidiosis as compared with non-infected ones. Also, the means of WBCs, N, L, M, E, and B among infected Gp1 and Gp2 were higher than the non-infected ones and these results were in agreement with that reported by Khan (2020). Also, the present study revealed higher N, L, M, and B among infected Gp2 compared to Gp1 [(45.61 vs. 49.61 N), (43.53 vs. 46.33 L), (6.18 vs. 6 B.53 M), and (0.8 vs. 0.83 B)]. A previous study attributed that to host defense mechanism against cryptosporidiosis, Water Harp⁶⁰. Another study done in Australia, Horn et al⁶¹ reported that WBC contribute indirectly to performance by keeping athletes’ infection free to maintain their training programs. Also, that study revealed that the more aerobic the sport, the lower the total WBC, N and M counts and these results were in consistence to our study.

In conclusion, this study revealed a high prevalence rate of IPIs among young swimmers in Alexandria. Helicobacter pylori, Blastocystis spp., and Cryptosporidium spp. were among the parasites found. Swimming habits, frequency, and duration of swimming dramatically affected the infectious status of swimmers. Furthermore, IPIs rates can also influence the state of immunity and anemia that may eventually cause abnormal BP and HR. Therefore, measures have been adopted to curb this problem by increasing the awareness of the importance of swimmers’ hygiene and targeted health education. Further studies with a longer follow-up period are necessary to investigate the effects of different interventions on the eradication of intestinal parasites among swimmers.

Funding:

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Conflict of interest:

The authors declare that they have no conflict of interest.

Acknowledgment:

The authors are thoroughly thankful to the administration of the club for their kind co-operation and support in obtaining the samples from the young swimmers. The authors are also grateful to parents for accepting the participation of their young swimmers in the study. Finally, special thanks also go to the study participants.

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No competing interests reported.

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Microbial Bowel Infections-Induced Biochemical and Biological Abnormalities among Young Egyptian Swimmers: Associated Risk Factors Affecting Swimming Performance Running title: Swimmers’ Microbial Bowel Infections and Swimming Performance

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