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Prevalence of urinary symptoms and infections among traditional tannery workers in the Fez city of Morocco: case–control study

Prevalence of urinary symptoms and infections among traditional tannery workers in the Fez city... Background: Many work activities such as leather tanning include hazards to work. Among these, biological hazards are particularly important and pose a serious problem to human health and environment. The aims of this study were to estimate the prevalence of dysuria and urinary tract infections among tannery workers and to identify their risk factors. Methods: This observational survey was conducted among 220 tannery workers and 220 age-matched control group from Fez city in Morocco. Reported urinary symptoms, demographic and professional information were obtained by a standardized questionnaire collected from participants and were then compared among the two groups. The logistic regression model was used to explore the interaction between variables with significant association. Results: The most common symptoms reported by tannery workers and controls were dysuria (36.4% vs. 1.8%, p < 0.001), voiding frequency (15.5% vs. 0.9%, p < 0.001) and incontinence (3.2% vs. 0.5%, p < 0.001). A positive urinary culture was seen in 3.64% of the tannery workers but not in the controls (0%). E-coli was the only species. Multivari- ate logistic regression showed that exposure to biological hazards increased significantly the odds of dysuria by 6.76 times (CI 1.112–41.78; p = 0.038) but rather, low or normal weight was a protective factor of dysuria (OR 0.53; CI 0.249–0.950; p = 0.035). Conclusion: Multiple working conditions including exposure to biological hazards may cause an increase in uro- genital disorders in the tannery workers. A significantly higher prevalence of urinary symptoms among male workers demand serious attention and further investigation. Keywords: Biological hazards, Dysuria, Tannery workers, Risk factors, Urinary tract infection 1 Background Recently, infectious diseases including microorganisms have been identified as the most common occupational diseases [22]. In the tanning sector, the processing of animal hides requires significant water usage, causing a *Correspondence: ilham.arhoune@usmba.ac.ma; arhoune.ilham@gmail.com Laboratory of Biomedical and Translational Research, Faculty high humidity working environment, when combined of Medicine, Sidi Mohammed Ben Abdellah University, KM 2.200 Road Sidi with elevated temperature and low oxygen concentra- Hrazem, Post Office Box 1893, 30070 Fez, Morocco tion, the high-humidity environment acts as a catalyst for Full list of author information is available at the end of the article © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Ilham et al. Afr J Urol (2021) 27:136 Page 2 of 7 microbial growth [3, 11]. The raw skins containing car -2.2 Data collection bohydrates, fats and proteins, as well as a high moisture For each participant, demographic data including age, content, provide an ideal medium for the rapid reproduc- education level, marital status and smoking habits were tion of microorganisms [18]. In addition to the working investigated. Other occupational conditions including environment and raw skins, some tannery agents, such duration of work, exposure to biological hazards (raw as oils, greases, pigeon dungs, and protein binders, also skins and pigeon dungs that may be contaminated with provide nutrients for microorganism propagation [8, 13]. a variety of bacteria, molds, virus, yeasts and various dis- An association between infectious diseases, humidity and eases), working environment: humid area (tasks in the temperature has been established because most of bacte- basins) and dry place (tasks far from the basins) were ria and fungi require specific environmental conditions to collected from the tannery workers by a questionnaire- proliferate [19]. The most frequent bacteria isolated from based interview. Participant tanners were also asked to hides and skins delivered directly to the tannery without determine the status of the use of Personal Protective prior treatment include: Escherichia coli, Staphylococ- Equipment (PPE) regarding boots and gloves. In addition, cus epidermidis, Morganella morganii, Proteus mirabi- Urinary Tract symptoms (UTS) and related hygienic con- lis, Proteus vulgaris, Bacillus anthracis, Bacillus subtilis, ditions were also collected including a total of 7 questions Pseudomonas aeruginosa, Lactobacillus Jensen and Bacil- (increased daytime frequency, nocturia, urgency, incon- lus mycoides [3, 19]. The possibility of contracting urinary tinence, dysuria, frequency of toilet break access and infection is a constant hazard for the tannery workers, use tissue/water after toilet). The personal medical his - because the animal skin and leather product contain tory including blood pressure (BP) and body mass index many microorganisms that have been identified in uro - (BMI) of participants  were measured following standard genital diseases [20]. For example, Escherichia coli and procedures. This index classifies the nutritional status of Enterobacter species can cause urinary tract infection, the subject into four categories: underweight < 18.5  kg/ 2 2 wound infection and abscesses septicaemia. m , normal 18.5–24.9  kg/m , overweight 25.0–29.9  kg/ 2 2 Symptoms of urinary tract infection (UTI), particularly m and obese ≥ 30 kg/m . dysuria, become more prevalent in men with increasing age. Although many physicians equate dysuria with UTI, 2.3 Sample collection it is actually a symptom that has many potential causes. The participants were asked to provide a fresh 10 ml spot Any source of irritation or inflammation of the urinary urine sample in the morning of a normal working day. tract, particularly the bladder, prostate or urethra, can The urine cytology was quantitatively performed using cause dysuria [2, 9]. It is difficult to draw conclusions the Sysmex UF-1000i urinary system (TOA Medical Elec- about causes from comparisons of symptoms. However, tronics, Kobe, Japan) to estimate white blood cell (WBC) such comparisons are useful in describing the subjects- count, red blood cell (RBC) count and bacteria. All urine perceived problems, and within country analyses may samples were examined on the same day as the urine help to improve methods for the study of urological samples were delivered. conditions. Therefore, information on biological hazards related 2.4 Microbiological analysis to urinary tracts in tannery workers has not been widely Urines were cultured and incubated at 37  °C for 24  h. researched, which justifies this study and demonstrates Presumptive Enterobacteriaceae (oxidase-negative, fac- its importance. Therefore, this study was designed to esti - ultative aerobic, Gram-negative rods) were identified by mate the prevalence of urinary symptoms and urinary using the API 20E system (bioMérieux, Marcy-l’Étoile, tract infection in tannery workers and to identify associ- France) and confirmed by method automated on Phoe - ated factors. nix. Antimicrobial susceptibility was determined as rec- ommended by the French Society of Microbiology (SFM, 2 Methods 2013). 2.1 S tudy design and participants UCBE interpretation was performed according to the This case–control study was conducted in traditional guidelines mentioned in the medical microbiology guide- tanneries of Fez city in Morocco from September 2017 4 lines (REMIC) [15]. More than 10 cells/ml was consid- to March 2018. It has included 220 male tannery workers ered as abnormal value for the number of average RBC aged ≥ 18  years having at least one year of work experi- and WBC in the urine. ence, and 220 age-matched male subject (control group). A participant was diagnosed as having a UTI if they The selection of the control group was collected ran - had clinical symptoms of UTI and the urinalysis showed domly from different activities (textile workers, adminis - bacteria (bacteriuria). Significant bacteriuria was defined trative personnel and sellers in the informal sectors). I lham et al. Afr J Urol (2021) 27:136 Page 3 of 7 as ≥ 10 colony-forming units (CFUs)/ml of a single bac- Table 1 Comparison of general characteristics between tannery workers and control group terial species in a freshly voided sample of urine as men- tioned in the 2015 French guidelines [5]. Characteristics of the Tannery Control p-value study population workers group n = 220 n = 220 (%) (%) 2.5 Data analysis The descriptive statistics technique was used for the Age (years) description of demographic variables. The prevalence 18–40 62 (28.2) 84 (38.2) 0.063 of urinary symptoms and UTI were reported. The Chi- 41–60 116 (52.7) 105 (47.7) square test was used to establish the possible associa- > 60 42 (19.1) 31 (14.1) tions between the presence of dysuria, demographic and BMI (Kg/m ) occupational parameters. Parameters with p < 0.05 were Underweight-normal 117 (62.2) 93 (52.5) 0.039 considered statistically significant. The binary logis - Overweight-obesity 71 (37.8) 84 (47.5) tic regression model was used as a multivariate analysis Educational level to determine the factors related to dysuria. Data analy- Illiterate 74 (33.6) 53 (24.1) 0.018 sis was performed using the statistical software package Literate 146 (66.4) 167 (75.9) SPSS 17.0. Marital status Unmarried 34 (15.5) 29 (13.2) 0.230 3 Results Married 186 (84.5) 191 (86.8) 3.1 G eneral characteristics, prevalence of urinary Smoking symptoms and hygienic conditions among tannery Yes 64 (29.1) 46 (20.9) 0.610 workers and control group No 156 (70.9) 174 (79.1) Data collection in the current study was completed from Biological hazards exposure 220 tannery workers and 220 control group. Demo- Yes 162 (73.6) – – graphic, clinical history and occupational characteris- No 58 (26.4) – tics of the two groups are presented in Table  1. Results PPE use showed that more than half of tannery workers (52.7%) Yes 56 (25.5) – – were between 40 and 60  years of age, 28.2% were rela- No 153 (69.5) – tively young and 84.5% were married. Then, they were Working area – likely to be more sexually active. No significant difference Humid area 159 (72.3) – – was found between tannery workers and controls with Dry place 61 (27.7) – respect to age, smoking habit and marital status. Smok- History of clinical conditions ing was slightly more frequent in tannery workers than Diabetes 11 (5.0) 21 (9.5) 0.049 the control group (29.1% vs. 20.9%, p = 0.61). Primar y High blood pressure (HBP) 34 (15.5) 20 (9.1) 0.029 school was the most prevalent education level in tannery PPE personal protective equipment workers (49.5%) compared to control group (28.2%). For occupational parameters, the majority of tannery work- ers (72.3%) were involved in a humid area in these tan- 3.2 UCBE results neries. Moreover, 73.6% of them were exposed to various The results of UCBE are displayed in Table  3. A sig- biological hazards and 69.5% of them they did not use nificant number of tannery workers had ≥ 10 RBCs any type of professional protective equipment. (hematuria) and ≥ 10 WBCs (leucocyturia) in their Table  2 shows that the tannery workers had a higher urine, where the number of hematuria and leucocyturia prevalence of many urinary symptoms and related work in tannery workers was higher than those of the con- conditions, except for nocturia which was significantly trol group (22.7% vs. 1.8%, p < 0.001 and 10.9% vs. 1.8%, higher in the control group. p < 0.001; respectively). Urinary tract infection was In particular, tannery workers had a significantly higher detected among 8 (3.64%) of the tannery workers but prevalence of dysuria compared to controls (36.4% vs. not in the controls (0%). 1.8%, p < 0.001). No significant difference was found in E. coli was the unique species isolated from the tan- the prevalence of urinary incontinence between the two nery workers having a positive culture. Chi-square-test groups. In terms of toilet access and hygiene measures, results of urinary parameters showed significant differ - about half of tannery workers (49.1%) and 40.4% of com- ences between the tannery workers and controls, which parison group require 3 or more toilet breaks in a day. indicates that tannery workers had a higher risk of uri- Moreover, very few of them reported they did not use tis- nary system abnormalities than those of the controls sue/water after using a toilet. Ilham et al. Afr J Urol (2021) 27:136 Page 4 of 7 Table 2 Prevalence and comparison of urine analysis results of dysuria in tannery workers, are indexed in Table  4 among the two groups and considered as candidate variables to the multivari- ate analysis. In terms of age, workers being more than Parameters Tannery workers Control group p-value (n = 220), n (%) (n = 220), n (%) 40  years showed more urinary symptoms than young ones. However, the Chi-square test shows no significant RBC relationship between age and dysuria (p = 0.27). A statis- (Cells/ml) tically significant relationship was established between > 10 50 (22.7) 4 (1.8) < 0.001 BMI and dysuria (p = 0.018). Moreover, the educational ≤ 10 170 (77.3) 216 (98.2) level, marital status, smoking habits and diabetes do WBC not affect the reported dysuria in tannery workers. The (Cells/ml) statistically significant predictors of dysuria were bio - ≥ 10 24 (10.9) 4 (1.8) < 0.001 logical hazards exposure (p = 0.003) and working area < 10 196 (89.1) 216 (98.2) (p = 0.017). Since the tannery workers had direct expo- Bacteria sure to biological hazards without appropriate PPE, CFU/ml ≥ 10 8 (3.64) 0 (0) < 0.001 < 10 212 (96.36) 220 (100) Table 4 Association between dysuria in tannery workers, Bold text indicates a statistically significant difference with a p-value less than demographic and professional characteristics 0.05 RBC red blood cells, WBC white blood cells Variables PS+ PS− p-value Age (years) 0.270 Table 3 Prevalence of urinary symptoms and hygienic ≤ 40 25 (40.3) 37 (59.7) conditions for tannery workers and control group > 40 55 (34.8) 103 (65.2) Urinary symptoms Tannery Control group n (%) p-value BMI (Kg/m ) 0.018 workers n Low-normal 53 (42.7) 71 (53.3) (%) Overweight-obesity 27 (28.1) 69 (71.9) Dysuria 80 (36.4) 4 (1.8) < 0.001 Educational level 0.230 Incontinence 18 (8.2) 16 (7.3) 0.430 Illiterate 24 (32.4) 50 (67.6) Nocturia (≥ 3 time/ 15 (6.8) 38 (17.3) 0.001 Literate 56 (38.4) 90 (61.6) night) Marital status 0.491 Toilet break access (time/ 0.021 Unmarried 10 (34.5) 19 (65.5) day) Married 70 (36.6) 121 (63.4) 0 0 (0) 6 (2.7) Smoking 0.350 1–2 112 (50.9) 125 (56.8) Yes 25 (39.1) 39 (60.9) 3 59 (26.8) 54 (24.5) No 55 (35.3) 101 (64.7) ≥ 4 49 (22.3) 35 (15.9) Biological hazards exposure 0.003 Use tissue/water after 0.002 toilet Yes 68 (42.0) 94 (58.0) 0.003 Yes 194 (88.2) 211(95.9) No 12 (20.7) 46 (79.3) No 26 (11.8) 9 (4.1) PPE uses 0.425 a Yes 4 (44.4) 5 (44.6) Subjects may have more than one urinary symptom No 76 (36.0) 135 (64.0) Working area 0.017 Humid area 65 (40.89) 94 (59.11) (Table  3). Multivariate logistic regression of urinary Dry place 15 (24.59) 46 (75.41) tract confirmed by bacteriological examination, socio- Diabetes demographic and occupational factors showed no asso- Yes 3 (27.3) 8 (72.7) 0.381 ciation in tannery workers and controls (p > 0.05). No 77 (36.8) 132 (63.2) High blood pressure (HBP) 0.027 3.3 A ssociation between socio-demographic parameters, Yes 7 (20.6) 27 (79.4) work conditions and the presence of dysuria No 73 (39.2) 113 (60.8) in tannery workers Bold text indicates a statistically significant difference with a p-value less than The results of the association between socio-demo - 0.05 graphic characteristics, work conditions and the presence PS+ , presence of dysuria I lham et al. Afr J Urol (2021) 27:136 Page 5 of 7 the Chi-square test shows no significant relationship after toilet. More than two thirds of tanners do not use between the use of PPE and the onset of the reported dys- any type of PPE. However, they reported that the use of uria (p = 0.425). Workers who have high blood pressure PPE was impractical due to the high humidity in Moroc- (HBP) are not the most affected by dysuria symptom. In can artisanal tanneries, especially in summer. The high spite of this, Chi-square test represents a statistically sig- rate of low educational level as one of the factor limited nificant relationship between the presence of HBP and knowledge about the existing health hazards and safety reported dysuria (p = 0.027). risks at work. Thus, they are at increased risk of contami - nants from all possible routes including the oral, inhala- 3.4 Multiv ariate logistic regression analysis of factors tion, ocular and dermal. associated with dysuria in tannery workers, Regarding voiding problems, the results of our study demographic characteristics and work conditions showed a significant difference urinary tract symptoms The logistic regression model was used to explore the (UTS) for voiding problems including dysuria and uri- interaction between variables with significant associa - nary frequency between the tannery workers and con- tion with dysuria symptom in the Chi-square test already trol group. It is true that UTS are not specific and can be done (Table  5). In this step, a logistic regression model increased by factors unrelated to prostatic conditions, has been conducted to explore the interaction between fluid intake, including diet and alcohol intake [1, 23, parameters with a significant association with dysuria in 26]. The finding may sound alarming because many of the Chi-square test already done. The OR brut and OR them report that they suffer from burning urination and adjusted have been compared to each selected variable. uncontrollable urine loss during work. Out of 111 (55%) Results showed that exposure to biological hazards was tannery workers with urinary symptoms, 3.67% had the major risk factor that increased 6 times or more the significant bacteriuria as confirmed by bacteriological risk of developing dysuria with (ORa = 6.76, CI = 1.107– examination. In comparison with symptomatic controls 41.349, p = 0.038). In contrast, having low or normal (1.8%), no bacteriuria were identified (0%). E. coli was weight (BMI < 25  kg/m2) was an independent protective the only specie isolated among tannery workers having factor of dysuria after adjusting which had an adjusted positive culture. Some infectious diseases such as UTI OR of 0.53 and a 95% CI of 0.249–0.950 (p = 0.035). caused by E. coli are common in the general population, which complicates the attribution to the workplace [14]. 4 Discussion According to the Biological Agent Biodefense Category The present study reports an important health issue on listed in the World Health Organization (WHO) and the urinary disorders among workers from traditional leather National Institute of Health (NIH), E. coli is a pathogen tanneries as well as compares these disorders with the that does not constitute a serious hazard to the com- control group. In terms of toilet access and hygiene meas- munity or to the environment [25]. On the other hand, ures, about half of tannery workers require 3 or more Chinese Laboratory Biosafety Categorization has classi- toilet breaks and the majority of them use tissue/water fied E. coli as a pathogenic agent that can spread easily Table 5 Comparison between ORb and ORa calculated by binary logistic regression for tannery workers Paramètre OR CI (95%) p OR CI (95%) p b a BMI (Kg/m ) ≤ 25 0.524 (0.297–0.927) 0.018 0.533 (0.249–0.950) 0.035* > 25 1 1 Humid area Yes 2.121 (1.366–5.268) 0.003 0.360 (0.063–2.075) 0.253 No 1 1 Biological hazards exposure Yes 2.773 (1.093–1.547) 0.017 6.76 (1.107–4.349) 0.038* No 1 1 HBP Yes 0.401 (0.166–0.969) 0.027 0.421 (0.168–1.050) 0.064 No 1 1 Bold text indicates a statistically significant difference with a p-value less than 0.05 OR , odds ratio brut; OR , odds ratio adjusted; CI, confidence interval b a Ilham et al. Afr J Urol (2021) 27:136 Page 6 of 7 between people, directly or indirectly, and can cause seri- working conditions were also found to be correlated ous human disease [25]. In the general population, there with increased risk of dysuria including working area are several causes of culture-negative urinary tract and exposure to biological hazards. These factors are sig - symptoms including antibiotics in urine, urinary tract nificant in bivariate analysis. The choice of the symptom malignancy, idiopathic interstitial cystitis, mycobacterial ’dysuria’ for logistic regression was due to the elevated infection, Schistosoma haematobium, fungal infection, rate of this symptom compared to others reported in the viral infection, inflammation or fastidious organisms current study. The multivariate logistic regression analy - [10]. A major factors that impact UTI incidence in our sis of factors associated with reported dysuria symptom study includes poor hygienic conditions, working in a investigates that exposure to biological hazards increased humid area and exposure to biological hazard especially, significantly the odds of dysuria by 6.76 times. How - in the traditional working environment. In agreement ever, having low or normal weight (BMI < 25 kg/m ) was with our study, poor sanitation, hygienic measures have a an independent protective factor of dysuria. In fact, it major influence on E. coli species [28]. However, protec - is difficult to draw a firm conclusion about causes from tion strategies, as well as monitoring, are recommended observational comparisons of symptoms. Nevertheless, for this community. such comparisons are useful in describing the workers- Urinalysis is a useful tool to identify not only infection, perceived problems in the traditional work environment, but also blood counts. In the current study, the hematu- to prevent various complications and improve working ria was significantly prevalent in the tannery population conditions. –3 compared to the control group (22.9% vs. 1.9%, p < 10 ). In this context, a significantly higher prevalence of uri - The prevalence of hematuria found in our control group nary symptoms among male workers demands a serious (1.9%) was lower than that reported in large previous attention and further investigation. The low number of screening studies among the general population which occupational diseases linked to biological agents should varied from 9 to 18% [12, 17, 21], particularly in the male not lead to an underestimation of biological risks, but population presenting to a health fair (8.6%) [6]. The should be used as a basis for a decision to reduce the multivariate analysis of factors associated with hematu- number of occupational risks. Since the exposure of tra- ria was conducted and showed no increased risk in the ditional tannery workers to biological agents cannot be tanners’ population. Previous risk factors identified of avoided, it will be reduced by the establishment of occu- urinary tract malignancy diagnosed following hematuria pational health program based on the development of were age, smoking, the presence of gross hematuria and inter-enterprise medical service (pre-employment and positive cytology [4, 17]. Moreover, diabetes and pro- periodic), the organization of medical surveillance pro- teinuria were also associated with hematuria in another gram and provision of information/training about haz- research [6]. ards and risks in the workplace. The prevalence of leucocyturia (WBC > 10 ), in the present study, was significantly higher in the tannery 5 Conclusion workers compared to that of the control group (10.9% The present study suggests that multiple working condi - –3 vs. 1.8%, p < 10 ). It was reported that the leukocyturia tions, including humid area and exposure to biological could suggest sterile pyuria and cannot reflect the possi - hazards, may cause an increase in the urinary tracts in bility of bacteriuria. However, main Clinical Associations the tannery workers. A significantly higher prevalence of including acute or chronic interstitial nephritis, prolif- urinary symptoms among male workers demands serious erative glomerulonephritis and urological disorders were attention and further investigation. In order to prevent reported [24]. In such cases, the correct interpretation of health issues among the tannery workers, we suggest the urinary findings requires adequate clinical informa - that medical observation, including pre-employment and tion and possibly renal biopsy. periodic medical controls, should be performed. Several studies have demonstrated that voiding symp- toms among men increase significantly with age and Acknowledgements This research work was carried out within the framework of an agreement functional disability [16, 21]. Other factors have been between the Faculty of Medicine and Pharmacy of Fez and the Ministry implicated in the dysuria progression including meta- of Tourism, Handicraft, Air Transport and Social Economy of Morocco. The bolic disorders [7]. Data from previous studies highlight authors are grateful to these two organizations for financial support. The authors also thank the respondents of the study. an association between high blood pressure, high BMI, diabetes and urinary disorders including dysuria [7, 23, Authors’ contributions 27]. In the present study, the risk to develop dysuria was AI conceived and designed the analysis, collected the data, contributed data or analysis tools, performed the analysis, and wrote the paper. HH conceived associated with different factors such as BMI and high and designed the analysis and collected the data. AB performed the analysis blood pressure but not necessarily age. Thus, multiple and critical revision of the article. BL collected the data and critically revised I lham et al. Afr J Urol (2021) 27:136 Page 7 of 7 the article. ES conceived and designed the analysis, contributed data or analy- 9. Fried M (2018) Dysuria. In: Sydney E, Weinstein E, Rucker LM (eds) Hand- sis tools and performed the analysis. AS conceived and designed the analysis, book of outpatient medicine. Springer International Publishing, Cham, pp critically revised the article, and was involved in the final approval of the revi- 451–464. https:// doi. org/ 10. 1007/ 978-3- 319- 68379-9_ 28 sion to be published. All authors have read and approved the manuscript. 10. Glover EK (2019) Urinary tract infection key points. Medicine 47(9):6–10. https:// doi. org/ 10. 1016/j. mpmed. 2019. 06. 008 Funding 11. Griffin DW (2007) Atmospheric movement of microorganisms in clouds Ministry of Crafts, Social Economy and Solidarity of Morocco. of desert dust and implications for human health. Clin Microbiol Rev 20(3):459–477 Availability of data and materials 12. Grossfeld GD, Litwin MS, Wolf JS, Hricak H, Shuler CL, Agerter DC, Carroll Not applicable. PR (2001) Evaluation of asymptomatic microscopic hematuria in adults: the American urological association best practice policy—partie: Defini- tion, detection, prevalence, and etiology. Urology 57(4):599–603 Declarations 13. Harchli EEH, Houssaini Iraqui M, Ibnsouda Koraichi S, Krishnan S (2015) Contribution À La Caractérisation Microbiologique et Enzymatique d’un Ethics approval and consent to participate Site Extrême : Les Tanneries Traditionnelles de Fès. Int J Eng Sci 5(2):16–24 The current survey was designed in accordance with legal requirements 14. Institut National de Recherche et de Sécurité (INRS) (2019) Les risques and the Declaration of Helsinki and was approved by the Joint Research biologiques en milieu professionnel Ethics Committee of Medical School and university Hospital Hassan II of Fez, 15. Lina G, Bonnet R, Bru J, Caron F, Cattoen C, Cattoir V, Courvalin P, Dubreuil Morocco (Number 29/16)”. People who accepted to participate in the study L, Jarlier V, Lefort A (2018) Comité de l’antibiogramme de la Société were requested to provide written informed consent. The UCBE analysis Française de Microbiologie Recommandations 2018 results were interpreted and delivered to the subjects confidentially. 16. Liu S, Chuang Y, Sumarsono B (2019) The prevalence and bother of lower urinary tract symptoms in men and women aged 40 years or over in Consent for publication Taiwan. J Formosan Med Assoc 118(1):170–178. https:// doi. org/ 10. 1016/j. Not applicable. jfma. 2018. 03. 006 17. 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Prevalence of urinary symptoms and infections among traditional tannery workers in the Fez city of Morocco: case–control study

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Abstract

Background: Many work activities such as leather tanning include hazards to work. Among these, biological hazards are particularly important and pose a serious problem to human health and environment. The aims of this study were to estimate the prevalence of dysuria and urinary tract infections among tannery workers and to identify their risk factors. Methods: This observational survey was conducted among 220 tannery workers and 220 age-matched control group from Fez city in Morocco. Reported urinary symptoms, demographic and professional information were obtained by a standardized questionnaire collected from participants and were then compared among the two groups. The logistic regression model was used to explore the interaction between variables with significant association. Results: The most common symptoms reported by tannery workers and controls were dysuria (36.4% vs. 1.8%, p < 0.001), voiding frequency (15.5% vs. 0.9%, p < 0.001) and incontinence (3.2% vs. 0.5%, p < 0.001). A positive urinary culture was seen in 3.64% of the tannery workers but not in the controls (0%). E-coli was the only species. Multivari- ate logistic regression showed that exposure to biological hazards increased significantly the odds of dysuria by 6.76 times (CI 1.112–41.78; p = 0.038) but rather, low or normal weight was a protective factor of dysuria (OR 0.53; CI 0.249–0.950; p = 0.035). Conclusion: Multiple working conditions including exposure to biological hazards may cause an increase in uro- genital disorders in the tannery workers. A significantly higher prevalence of urinary symptoms among male workers demand serious attention and further investigation. Keywords: Biological hazards, Dysuria, Tannery workers, Risk factors, Urinary tract infection 1 Background Recently, infectious diseases including microorganisms have been identified as the most common occupational diseases [22]. In the tanning sector, the processing of animal hides requires significant water usage, causing a *Correspondence: ilham.arhoune@usmba.ac.ma; arhoune.ilham@gmail.com Laboratory of Biomedical and Translational Research, Faculty high humidity working environment, when combined of Medicine, Sidi Mohammed Ben Abdellah University, KM 2.200 Road Sidi with elevated temperature and low oxygen concentra- Hrazem, Post Office Box 1893, 30070 Fez, Morocco tion, the high-humidity environment acts as a catalyst for Full list of author information is available at the end of the article © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Ilham et al. Afr J Urol (2021) 27:136 Page 2 of 7 microbial growth [3, 11]. The raw skins containing car -2.2 Data collection bohydrates, fats and proteins, as well as a high moisture For each participant, demographic data including age, content, provide an ideal medium for the rapid reproduc- education level, marital status and smoking habits were tion of microorganisms [18]. In addition to the working investigated. Other occupational conditions including environment and raw skins, some tannery agents, such duration of work, exposure to biological hazards (raw as oils, greases, pigeon dungs, and protein binders, also skins and pigeon dungs that may be contaminated with provide nutrients for microorganism propagation [8, 13]. a variety of bacteria, molds, virus, yeasts and various dis- An association between infectious diseases, humidity and eases), working environment: humid area (tasks in the temperature has been established because most of bacte- basins) and dry place (tasks far from the basins) were ria and fungi require specific environmental conditions to collected from the tannery workers by a questionnaire- proliferate [19]. The most frequent bacteria isolated from based interview. Participant tanners were also asked to hides and skins delivered directly to the tannery without determine the status of the use of Personal Protective prior treatment include: Escherichia coli, Staphylococ- Equipment (PPE) regarding boots and gloves. In addition, cus epidermidis, Morganella morganii, Proteus mirabi- Urinary Tract symptoms (UTS) and related hygienic con- lis, Proteus vulgaris, Bacillus anthracis, Bacillus subtilis, ditions were also collected including a total of 7 questions Pseudomonas aeruginosa, Lactobacillus Jensen and Bacil- (increased daytime frequency, nocturia, urgency, incon- lus mycoides [3, 19]. The possibility of contracting urinary tinence, dysuria, frequency of toilet break access and infection is a constant hazard for the tannery workers, use tissue/water after toilet). The personal medical his - because the animal skin and leather product contain tory including blood pressure (BP) and body mass index many microorganisms that have been identified in uro - (BMI) of participants  were measured following standard genital diseases [20]. For example, Escherichia coli and procedures. This index classifies the nutritional status of Enterobacter species can cause urinary tract infection, the subject into four categories: underweight < 18.5  kg/ 2 2 wound infection and abscesses septicaemia. m , normal 18.5–24.9  kg/m , overweight 25.0–29.9  kg/ 2 2 Symptoms of urinary tract infection (UTI), particularly m and obese ≥ 30 kg/m . dysuria, become more prevalent in men with increasing age. Although many physicians equate dysuria with UTI, 2.3 Sample collection it is actually a symptom that has many potential causes. The participants were asked to provide a fresh 10 ml spot Any source of irritation or inflammation of the urinary urine sample in the morning of a normal working day. tract, particularly the bladder, prostate or urethra, can The urine cytology was quantitatively performed using cause dysuria [2, 9]. It is difficult to draw conclusions the Sysmex UF-1000i urinary system (TOA Medical Elec- about causes from comparisons of symptoms. However, tronics, Kobe, Japan) to estimate white blood cell (WBC) such comparisons are useful in describing the subjects- count, red blood cell (RBC) count and bacteria. All urine perceived problems, and within country analyses may samples were examined on the same day as the urine help to improve methods for the study of urological samples were delivered. conditions. Therefore, information on biological hazards related 2.4 Microbiological analysis to urinary tracts in tannery workers has not been widely Urines were cultured and incubated at 37  °C for 24  h. researched, which justifies this study and demonstrates Presumptive Enterobacteriaceae (oxidase-negative, fac- its importance. Therefore, this study was designed to esti - ultative aerobic, Gram-negative rods) were identified by mate the prevalence of urinary symptoms and urinary using the API 20E system (bioMérieux, Marcy-l’Étoile, tract infection in tannery workers and to identify associ- France) and confirmed by method automated on Phoe - ated factors. nix. Antimicrobial susceptibility was determined as rec- ommended by the French Society of Microbiology (SFM, 2 Methods 2013). 2.1 S tudy design and participants UCBE interpretation was performed according to the This case–control study was conducted in traditional guidelines mentioned in the medical microbiology guide- tanneries of Fez city in Morocco from September 2017 4 lines (REMIC) [15]. More than 10 cells/ml was consid- to March 2018. It has included 220 male tannery workers ered as abnormal value for the number of average RBC aged ≥ 18  years having at least one year of work experi- and WBC in the urine. ence, and 220 age-matched male subject (control group). A participant was diagnosed as having a UTI if they The selection of the control group was collected ran - had clinical symptoms of UTI and the urinalysis showed domly from different activities (textile workers, adminis - bacteria (bacteriuria). Significant bacteriuria was defined trative personnel and sellers in the informal sectors). I lham et al. Afr J Urol (2021) 27:136 Page 3 of 7 as ≥ 10 colony-forming units (CFUs)/ml of a single bac- Table 1 Comparison of general characteristics between tannery workers and control group terial species in a freshly voided sample of urine as men- tioned in the 2015 French guidelines [5]. Characteristics of the Tannery Control p-value study population workers group n = 220 n = 220 (%) (%) 2.5 Data analysis The descriptive statistics technique was used for the Age (years) description of demographic variables. The prevalence 18–40 62 (28.2) 84 (38.2) 0.063 of urinary symptoms and UTI were reported. The Chi- 41–60 116 (52.7) 105 (47.7) square test was used to establish the possible associa- > 60 42 (19.1) 31 (14.1) tions between the presence of dysuria, demographic and BMI (Kg/m ) occupational parameters. Parameters with p < 0.05 were Underweight-normal 117 (62.2) 93 (52.5) 0.039 considered statistically significant. The binary logis - Overweight-obesity 71 (37.8) 84 (47.5) tic regression model was used as a multivariate analysis Educational level to determine the factors related to dysuria. Data analy- Illiterate 74 (33.6) 53 (24.1) 0.018 sis was performed using the statistical software package Literate 146 (66.4) 167 (75.9) SPSS 17.0. Marital status Unmarried 34 (15.5) 29 (13.2) 0.230 3 Results Married 186 (84.5) 191 (86.8) 3.1 G eneral characteristics, prevalence of urinary Smoking symptoms and hygienic conditions among tannery Yes 64 (29.1) 46 (20.9) 0.610 workers and control group No 156 (70.9) 174 (79.1) Data collection in the current study was completed from Biological hazards exposure 220 tannery workers and 220 control group. Demo- Yes 162 (73.6) – – graphic, clinical history and occupational characteris- No 58 (26.4) – tics of the two groups are presented in Table  1. Results PPE use showed that more than half of tannery workers (52.7%) Yes 56 (25.5) – – were between 40 and 60  years of age, 28.2% were rela- No 153 (69.5) – tively young and 84.5% were married. Then, they were Working area – likely to be more sexually active. No significant difference Humid area 159 (72.3) – – was found between tannery workers and controls with Dry place 61 (27.7) – respect to age, smoking habit and marital status. Smok- History of clinical conditions ing was slightly more frequent in tannery workers than Diabetes 11 (5.0) 21 (9.5) 0.049 the control group (29.1% vs. 20.9%, p = 0.61). Primar y High blood pressure (HBP) 34 (15.5) 20 (9.1) 0.029 school was the most prevalent education level in tannery PPE personal protective equipment workers (49.5%) compared to control group (28.2%). For occupational parameters, the majority of tannery work- ers (72.3%) were involved in a humid area in these tan- 3.2 UCBE results neries. Moreover, 73.6% of them were exposed to various The results of UCBE are displayed in Table  3. A sig- biological hazards and 69.5% of them they did not use nificant number of tannery workers had ≥ 10 RBCs any type of professional protective equipment. (hematuria) and ≥ 10 WBCs (leucocyturia) in their Table  2 shows that the tannery workers had a higher urine, where the number of hematuria and leucocyturia prevalence of many urinary symptoms and related work in tannery workers was higher than those of the con- conditions, except for nocturia which was significantly trol group (22.7% vs. 1.8%, p < 0.001 and 10.9% vs. 1.8%, higher in the control group. p < 0.001; respectively). Urinary tract infection was In particular, tannery workers had a significantly higher detected among 8 (3.64%) of the tannery workers but prevalence of dysuria compared to controls (36.4% vs. not in the controls (0%). 1.8%, p < 0.001). No significant difference was found in E. coli was the unique species isolated from the tan- the prevalence of urinary incontinence between the two nery workers having a positive culture. Chi-square-test groups. In terms of toilet access and hygiene measures, results of urinary parameters showed significant differ - about half of tannery workers (49.1%) and 40.4% of com- ences between the tannery workers and controls, which parison group require 3 or more toilet breaks in a day. indicates that tannery workers had a higher risk of uri- Moreover, very few of them reported they did not use tis- nary system abnormalities than those of the controls sue/water after using a toilet. Ilham et al. Afr J Urol (2021) 27:136 Page 4 of 7 Table 2 Prevalence and comparison of urine analysis results of dysuria in tannery workers, are indexed in Table  4 among the two groups and considered as candidate variables to the multivari- ate analysis. In terms of age, workers being more than Parameters Tannery workers Control group p-value (n = 220), n (%) (n = 220), n (%) 40  years showed more urinary symptoms than young ones. However, the Chi-square test shows no significant RBC relationship between age and dysuria (p = 0.27). A statis- (Cells/ml) tically significant relationship was established between > 10 50 (22.7) 4 (1.8) < 0.001 BMI and dysuria (p = 0.018). Moreover, the educational ≤ 10 170 (77.3) 216 (98.2) level, marital status, smoking habits and diabetes do WBC not affect the reported dysuria in tannery workers. The (Cells/ml) statistically significant predictors of dysuria were bio - ≥ 10 24 (10.9) 4 (1.8) < 0.001 logical hazards exposure (p = 0.003) and working area < 10 196 (89.1) 216 (98.2) (p = 0.017). Since the tannery workers had direct expo- Bacteria sure to biological hazards without appropriate PPE, CFU/ml ≥ 10 8 (3.64) 0 (0) < 0.001 < 10 212 (96.36) 220 (100) Table 4 Association between dysuria in tannery workers, Bold text indicates a statistically significant difference with a p-value less than demographic and professional characteristics 0.05 RBC red blood cells, WBC white blood cells Variables PS+ PS− p-value Age (years) 0.270 Table 3 Prevalence of urinary symptoms and hygienic ≤ 40 25 (40.3) 37 (59.7) conditions for tannery workers and control group > 40 55 (34.8) 103 (65.2) Urinary symptoms Tannery Control group n (%) p-value BMI (Kg/m ) 0.018 workers n Low-normal 53 (42.7) 71 (53.3) (%) Overweight-obesity 27 (28.1) 69 (71.9) Dysuria 80 (36.4) 4 (1.8) < 0.001 Educational level 0.230 Incontinence 18 (8.2) 16 (7.3) 0.430 Illiterate 24 (32.4) 50 (67.6) Nocturia (≥ 3 time/ 15 (6.8) 38 (17.3) 0.001 Literate 56 (38.4) 90 (61.6) night) Marital status 0.491 Toilet break access (time/ 0.021 Unmarried 10 (34.5) 19 (65.5) day) Married 70 (36.6) 121 (63.4) 0 0 (0) 6 (2.7) Smoking 0.350 1–2 112 (50.9) 125 (56.8) Yes 25 (39.1) 39 (60.9) 3 59 (26.8) 54 (24.5) No 55 (35.3) 101 (64.7) ≥ 4 49 (22.3) 35 (15.9) Biological hazards exposure 0.003 Use tissue/water after 0.002 toilet Yes 68 (42.0) 94 (58.0) 0.003 Yes 194 (88.2) 211(95.9) No 12 (20.7) 46 (79.3) No 26 (11.8) 9 (4.1) PPE uses 0.425 a Yes 4 (44.4) 5 (44.6) Subjects may have more than one urinary symptom No 76 (36.0) 135 (64.0) Working area 0.017 Humid area 65 (40.89) 94 (59.11) (Table  3). Multivariate logistic regression of urinary Dry place 15 (24.59) 46 (75.41) tract confirmed by bacteriological examination, socio- Diabetes demographic and occupational factors showed no asso- Yes 3 (27.3) 8 (72.7) 0.381 ciation in tannery workers and controls (p > 0.05). No 77 (36.8) 132 (63.2) High blood pressure (HBP) 0.027 3.3 A ssociation between socio-demographic parameters, Yes 7 (20.6) 27 (79.4) work conditions and the presence of dysuria No 73 (39.2) 113 (60.8) in tannery workers Bold text indicates a statistically significant difference with a p-value less than The results of the association between socio-demo - 0.05 graphic characteristics, work conditions and the presence PS+ , presence of dysuria I lham et al. Afr J Urol (2021) 27:136 Page 5 of 7 the Chi-square test shows no significant relationship after toilet. More than two thirds of tanners do not use between the use of PPE and the onset of the reported dys- any type of PPE. However, they reported that the use of uria (p = 0.425). Workers who have high blood pressure PPE was impractical due to the high humidity in Moroc- (HBP) are not the most affected by dysuria symptom. In can artisanal tanneries, especially in summer. The high spite of this, Chi-square test represents a statistically sig- rate of low educational level as one of the factor limited nificant relationship between the presence of HBP and knowledge about the existing health hazards and safety reported dysuria (p = 0.027). risks at work. Thus, they are at increased risk of contami - nants from all possible routes including the oral, inhala- 3.4 Multiv ariate logistic regression analysis of factors tion, ocular and dermal. associated with dysuria in tannery workers, Regarding voiding problems, the results of our study demographic characteristics and work conditions showed a significant difference urinary tract symptoms The logistic regression model was used to explore the (UTS) for voiding problems including dysuria and uri- interaction between variables with significant associa - nary frequency between the tannery workers and con- tion with dysuria symptom in the Chi-square test already trol group. It is true that UTS are not specific and can be done (Table  5). In this step, a logistic regression model increased by factors unrelated to prostatic conditions, has been conducted to explore the interaction between fluid intake, including diet and alcohol intake [1, 23, parameters with a significant association with dysuria in 26]. The finding may sound alarming because many of the Chi-square test already done. The OR brut and OR them report that they suffer from burning urination and adjusted have been compared to each selected variable. uncontrollable urine loss during work. Out of 111 (55%) Results showed that exposure to biological hazards was tannery workers with urinary symptoms, 3.67% had the major risk factor that increased 6 times or more the significant bacteriuria as confirmed by bacteriological risk of developing dysuria with (ORa = 6.76, CI = 1.107– examination. In comparison with symptomatic controls 41.349, p = 0.038). In contrast, having low or normal (1.8%), no bacteriuria were identified (0%). E. coli was weight (BMI < 25  kg/m2) was an independent protective the only specie isolated among tannery workers having factor of dysuria after adjusting which had an adjusted positive culture. Some infectious diseases such as UTI OR of 0.53 and a 95% CI of 0.249–0.950 (p = 0.035). caused by E. coli are common in the general population, which complicates the attribution to the workplace [14]. 4 Discussion According to the Biological Agent Biodefense Category The present study reports an important health issue on listed in the World Health Organization (WHO) and the urinary disorders among workers from traditional leather National Institute of Health (NIH), E. coli is a pathogen tanneries as well as compares these disorders with the that does not constitute a serious hazard to the com- control group. In terms of toilet access and hygiene meas- munity or to the environment [25]. On the other hand, ures, about half of tannery workers require 3 or more Chinese Laboratory Biosafety Categorization has classi- toilet breaks and the majority of them use tissue/water fied E. coli as a pathogenic agent that can spread easily Table 5 Comparison between ORb and ORa calculated by binary logistic regression for tannery workers Paramètre OR CI (95%) p OR CI (95%) p b a BMI (Kg/m ) ≤ 25 0.524 (0.297–0.927) 0.018 0.533 (0.249–0.950) 0.035* > 25 1 1 Humid area Yes 2.121 (1.366–5.268) 0.003 0.360 (0.063–2.075) 0.253 No 1 1 Biological hazards exposure Yes 2.773 (1.093–1.547) 0.017 6.76 (1.107–4.349) 0.038* No 1 1 HBP Yes 0.401 (0.166–0.969) 0.027 0.421 (0.168–1.050) 0.064 No 1 1 Bold text indicates a statistically significant difference with a p-value less than 0.05 OR , odds ratio brut; OR , odds ratio adjusted; CI, confidence interval b a Ilham et al. Afr J Urol (2021) 27:136 Page 6 of 7 between people, directly or indirectly, and can cause seri- working conditions were also found to be correlated ous human disease [25]. In the general population, there with increased risk of dysuria including working area are several causes of culture-negative urinary tract and exposure to biological hazards. These factors are sig - symptoms including antibiotics in urine, urinary tract nificant in bivariate analysis. The choice of the symptom malignancy, idiopathic interstitial cystitis, mycobacterial ’dysuria’ for logistic regression was due to the elevated infection, Schistosoma haematobium, fungal infection, rate of this symptom compared to others reported in the viral infection, inflammation or fastidious organisms current study. The multivariate logistic regression analy - [10]. A major factors that impact UTI incidence in our sis of factors associated with reported dysuria symptom study includes poor hygienic conditions, working in a investigates that exposure to biological hazards increased humid area and exposure to biological hazard especially, significantly the odds of dysuria by 6.76 times. How - in the traditional working environment. In agreement ever, having low or normal weight (BMI < 25 kg/m ) was with our study, poor sanitation, hygienic measures have a an independent protective factor of dysuria. In fact, it major influence on E. coli species [28]. However, protec - is difficult to draw a firm conclusion about causes from tion strategies, as well as monitoring, are recommended observational comparisons of symptoms. Nevertheless, for this community. such comparisons are useful in describing the workers- Urinalysis is a useful tool to identify not only infection, perceived problems in the traditional work environment, but also blood counts. In the current study, the hematu- to prevent various complications and improve working ria was significantly prevalent in the tannery population conditions. –3 compared to the control group (22.9% vs. 1.9%, p < 10 ). In this context, a significantly higher prevalence of uri - The prevalence of hematuria found in our control group nary symptoms among male workers demands a serious (1.9%) was lower than that reported in large previous attention and further investigation. The low number of screening studies among the general population which occupational diseases linked to biological agents should varied from 9 to 18% [12, 17, 21], particularly in the male not lead to an underestimation of biological risks, but population presenting to a health fair (8.6%) [6]. The should be used as a basis for a decision to reduce the multivariate analysis of factors associated with hematu- number of occupational risks. Since the exposure of tra- ria was conducted and showed no increased risk in the ditional tannery workers to biological agents cannot be tanners’ population. Previous risk factors identified of avoided, it will be reduced by the establishment of occu- urinary tract malignancy diagnosed following hematuria pational health program based on the development of were age, smoking, the presence of gross hematuria and inter-enterprise medical service (pre-employment and positive cytology [4, 17]. Moreover, diabetes and pro- periodic), the organization of medical surveillance pro- teinuria were also associated with hematuria in another gram and provision of information/training about haz- research [6]. ards and risks in the workplace. The prevalence of leucocyturia (WBC > 10 ), in the present study, was significantly higher in the tannery 5 Conclusion workers compared to that of the control group (10.9% The present study suggests that multiple working condi - –3 vs. 1.8%, p < 10 ). It was reported that the leukocyturia tions, including humid area and exposure to biological could suggest sterile pyuria and cannot reflect the possi - hazards, may cause an increase in the urinary tracts in bility of bacteriuria. However, main Clinical Associations the tannery workers. A significantly higher prevalence of including acute or chronic interstitial nephritis, prolif- urinary symptoms among male workers demands serious erative glomerulonephritis and urological disorders were attention and further investigation. In order to prevent reported [24]. In such cases, the correct interpretation of health issues among the tannery workers, we suggest the urinary findings requires adequate clinical informa - that medical observation, including pre-employment and tion and possibly renal biopsy. periodic medical controls, should be performed. Several studies have demonstrated that voiding symp- toms among men increase significantly with age and Acknowledgements This research work was carried out within the framework of an agreement functional disability [16, 21]. Other factors have been between the Faculty of Medicine and Pharmacy of Fez and the Ministry implicated in the dysuria progression including meta- of Tourism, Handicraft, Air Transport and Social Economy of Morocco. The bolic disorders [7]. Data from previous studies highlight authors are grateful to these two organizations for financial support. The authors also thank the respondents of the study. an association between high blood pressure, high BMI, diabetes and urinary disorders including dysuria [7, 23, Authors’ contributions 27]. In the present study, the risk to develop dysuria was AI conceived and designed the analysis, collected the data, contributed data or analysis tools, performed the analysis, and wrote the paper. HH conceived associated with different factors such as BMI and high and designed the analysis and collected the data. AB performed the analysis blood pressure but not necessarily age. Thus, multiple and critical revision of the article. BL collected the data and critically revised I lham et al. Afr J Urol (2021) 27:136 Page 7 of 7 the article. ES conceived and designed the analysis, contributed data or analy- 9. Fried M (2018) Dysuria. In: Sydney E, Weinstein E, Rucker LM (eds) Hand- sis tools and performed the analysis. AS conceived and designed the analysis, book of outpatient medicine. Springer International Publishing, Cham, pp critically revised the article, and was involved in the final approval of the revi- 451–464. https:// doi. org/ 10. 1007/ 978-3- 319- 68379-9_ 28 sion to be published. All authors have read and approved the manuscript. 10. Glover EK (2019) Urinary tract infection key points. Medicine 47(9):6–10. https:// doi. org/ 10. 1016/j. mpmed. 2019. 06. 008 Funding 11. Griffin DW (2007) Atmospheric movement of microorganisms in clouds Ministry of Crafts, Social Economy and Solidarity of Morocco. of desert dust and implications for human health. Clin Microbiol Rev 20(3):459–477 Availability of data and materials 12. Grossfeld GD, Litwin MS, Wolf JS, Hricak H, Shuler CL, Agerter DC, Carroll Not applicable. PR (2001) Evaluation of asymptomatic microscopic hematuria in adults: the American urological association best practice policy—partie: Defini- tion, detection, prevalence, and etiology. Urology 57(4):599–603 Declarations 13. Harchli EEH, Houssaini Iraqui M, Ibnsouda Koraichi S, Krishnan S (2015) Contribution À La Caractérisation Microbiologique et Enzymatique d’un Ethics approval and consent to participate Site Extrême : Les Tanneries Traditionnelles de Fès. Int J Eng Sci 5(2):16–24 The current survey was designed in accordance with legal requirements 14. Institut National de Recherche et de Sécurité (INRS) (2019) Les risques and the Declaration of Helsinki and was approved by the Joint Research biologiques en milieu professionnel Ethics Committee of Medical School and university Hospital Hassan II of Fez, 15. Lina G, Bonnet R, Bru J, Caron F, Cattoen C, Cattoir V, Courvalin P, Dubreuil Morocco (Number 29/16)”. People who accepted to participate in the study L, Jarlier V, Lefort A (2018) Comité de l’antibiogramme de la Société were requested to provide written informed consent. The UCBE analysis Française de Microbiologie Recommandations 2018 results were interpreted and delivered to the subjects confidentially. 16. Liu S, Chuang Y, Sumarsono B (2019) The prevalence and bother of lower urinary tract symptoms in men and women aged 40 years or over in Consent for publication Taiwan. J Formosan Med Assoc 118(1):170–178. https:// doi. org/ 10. 1016/j. Not applicable. jfma. 2018. 03. 006 17. 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Journal

African Journal of Urology – Springer Journals

Published: Dec 1, 2021

Keywords: Biological hazards; Dysuria; Tannery workers; Risk factors; Urinary tract infection

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