Lowy FD, 1998. Staphylococcus aureus infections. N Engl J Med 339: 520–532.
DeLeo FR, Otto M, Kreiswirth BN, Chambers HF, 2010. Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557–1568.
Chisti MJ, Tebruegge M, La Vincente S, Graham SM, Duke T, 2009. Pneumonia in severely malnourished children in developing countries: mortality risk, aetiology and validity of WHO clinical signs: a systematic review. Trop Med Int Health 14: 1173–1189.
Sigauque B, Roca A, Mandomando I, Morais L, Quintó L, Sacarlal J, Macete E, Nhamposa T, Machevo S, Aide P, Bassat Q, Bardají A, Nhalungo D, Soriano-Gabarró M, Flannery B, Menendez C, Levine MM, Alonso PL, 2009. Community-acquired bacteremia among children admitted to a rural hospital in Mozambique. Pediatr Infect Dis J 28: 108–113.
Wood SM, Shah SS, Bafana M, Ratner AJ, Meaney PA, Malefho KC, Steenhoff AP, 2009. Epidemiology of methicillin-resistant Staphylococcus aureus bacteremia in Gaborone, Botswana. Infect Control Hosp Epidemiol 30: 782–785.
Cotton MF, Wasserman E, Smit J, Whitelaw A, Zar HJ, 2008. High incidence of antimicrobial resistant organisms including extended spectrum beta-lactamase producing Enterobacteriaceae and methicillin-resistant Staphylococcus aureus in nasopharyngeal and blood isolates of HIV-infected children from Cape Town, South Africa. BMC Infect Dis 8: 40.
Singh V, Aneja S, 2011. Pneumonia: management in the developing world. Paediatr Respir Rev 12: 52–59.
Naidoo R, Nuttall J, Whitelaw A, Eley B, 2013. Epidemiology of Staphylococcus aureus bacteraemia at a tertiary children's hospital in Cape Town, South Africa. PLoS One 8: e78396.
Preidis GA, McCollum ED, Mwansambo C, Kazembe PN, Schutze GE, Kline MW, 2011. Pneumonia and malnutrition are highly predictive of mortality among African children hospitalized with human immunodeficiency virus infection or exposure in the era of antiretroviral therapy. J Pediatr 159: 484–489.
Ahmed AO, van Belkum A, Fahal AH, Elnor AE, Abougroun ES, VandenBergh MF, Zijlstra EE, Verbrugh HA, 1998. Nasal carriage of Staphylococcus aureus and epidemiology of surgical-site infections in a Sudanese university hospital. J Clin Microbiol 36: 3614–3618.
Kluytmans J, van Belkum A, Verbrugh H, 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10: 505–520.
Truong H, Shah SS, Ludmir J, Twananana EO, Bafana M, Wood SM, Moffat H, Steenhoff AP, 2011. Staphylococcus aureus skin and soft tissue infections at a tertiary hospital in Botswana. S Afr Med J 101: 413–416.
Shet A, Mathema B, Mediavilla JR, Kishii K, Mehandru S, Jeane-Pierre P, Laroche M, Willey BM, Kreiswirth N, Markowitz M, Kreiswirth BN, 2009. Colonization and subsequent skin and soft tissue infection due to methicillin-resistant Staphylococcus aureus in a cohort of otherwise healthy adults infected with HIV type 1. J Infect Dis 200: 88–93.
Miller M, Cespedes C, Bhat M, Vavagiakis P, Klein RS, Lowy FD, 2007. Incidence and persistence of Staphylococcus aureus nasal colonization in a community sample of HIV-infected and -uninfected drug users. Clin Infect Dis 45: 343–346.
National AIDS Coordinating Agency (NACA), 2013. Preliminary Results Botswana AIDS Impact Survey IV. Gaborone, Botswana: Statistics Botswana, 25.
Brown EL, Below JE, Fischer RS, Essigmann HT, Hu H, Huff C, Robinson DA, Petty LE, Aguilar D, Bell GI, Hanis CL, 2015. Genome-wide association study of Staphylococcus aureus carriage in a community-based sample of Mexican-Americans in Starr County, Texas. PLoS One 10: e0142130.
Leung NS, Padgett P, Robinson DA, Brown EL, 2015. Prevalence and behavioural risk factors of Staphylococcus aureus nasal colonization in community-based injection drug users. Epidemiol Infect 143: 2430–2439.
McAllister SK, Albrecht VS, Fosheim GE, Lowery HK, Peters PJ, Gorwitz R, Guest JL, Hageman J, Mindley R, McDougal LK, Rimland D, Limbago B, 2011. Evaluation of the impact of direct plating, broth enrichment, and specimen source on recovery and diversity of methicillin-resistant Staphylococcus aureus isolates among HIV-infected outpatients. J Clin Microbiol 49: 4126–4130.
Clinical Laboratory Standards Institute (CLSI), 2013. Performance Standards for Antimicrobial Susceptibility Testing. Twenty-Third Informational Supplement. CLSI Document M100-S23. Wayne, PA: CLSI.
European Committee on Antimicrobial Susceptibility Testing (EUCAST), 2016. Testing EC on AS. Antimicrobial Susceptibility Testing EUCAST Disk Breakpoint Tables for Interpretation of MICs and Zone Diameters, Version 3.0. Available at: http://www.eucast.org/ast_of_bacteria/. Accessed May 14, 2016.
Nouwen JL, Ott A, Kluytmans-Vandenbergh MF, Boelens HA, Hofman A, van Belkum A, Verbrugh HA, 2004. Predicting the Staphylococcus aureus nasal carrier state: derivation and validation of a “culture rule.” Clin Infect Dis 39: 806–811.
Barros AJ, Hirakata VN, 2003. Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 3: 21.
Coutinho LM, Scazufca M, Menezes PR, 2008. Methods for estimating prevalence ratios in cross-sectional studies. Rev Saude Publica 42: 992–998.
Zou G, 2004. A modified Poisson regression approach to prospective studies with binary data. Am J Epidemiol 159: 702–706.
McNally LM, Jeena PM, Gajee K, Sturm AW, Tomkins AM, Coovadia HM, Goldblatt D, 2006. Lack of association between the nasopharyngeal carriage of Streptococcus pneumoniae and Staphylococcus aureus in HIV-1-infected South African children. J Infect Dis 194: 385–390.
Madhi SA, Adrian P, Kuwanda L, Cutland C, Albrich WC, Klugman KP, 2007. Long-term effect of pneumococcal conjugate vaccine on nasopharyngeal colonization by Streptococcus pneumoniae—and associated interactions with Staphylococcus aureus and Haemophilus influenzae colonization—in HIV-infected and HIV-uninfected children. J Infect Dis 196: 1662–1666.
Bhattacharya SD, Niyogi SK, Bhattacharyya S, Arya BK, Chauhan N, Mandal S, 2012. Associations between potential bacterial pathogens in the nasopharynx of HIV infected children. Indian J Pediatr 79: 1447–1453.
Krcmery V, Sokolova J, Kulkova N, Liskova A, Shahum A, Benca G, 2013. Nasopharyngeal bacterial colonisation in HIV-positive children in Cambodia. Trop Med Int Health 18: 1267–1268.
Zervou FN, Zacharioudakis IM, Ziakas PD, Rich JD, Mylonakis E, 2014. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus colonization in HIV infection: a meta-analysis. Clin Infect Dis 59: 1302–1311.
Korenromp EL, Williams BG, Schmid GP, Dye C, 2009. Clinical prognostic value of RNA viral load and CD4 cell counts during untreated HIV-1 infection: a quantitative review. PLoS One 4: e5950.
Chambers HF, Hartman BJ, Tomasz A, 1985. Increased amounts of a novel penicillin-binding protein in a strain of methicillin-resistant Staphylococcus aureus exposed to nafcillin. J Clin Invest 76: 325–331.
Chambers HF, 1997. Methicillin resistance in staphylococci: molecular and biochemical basis and clinical implications. Clin Microbiol Rev 10: 781–791.
Dien Bard J, Hindler JA, Gold HS, Limbago B, 2014. Rationale for eliminating Staphylococcus breakpoints for beta-lactam agents other than penicillin, oxacillin or cefoxitin, and ceftaroline. Clin Infect Dis 58: 1287–1296.
Schaumburg F, Alabi AS, Peters G, Becker K, 2014. New epidemiology of Staphylococcus aureus infection in Africa. Clin Microbiol Infect 20: 589–596.
Maalej SM, Rhimi FM, Fines M, Mnif B, Leclercq R, Hammami A, 2012. Analysis of borderline oxacillin-resistant Staphylococcus aureus (BORSA) strains isolated in Tunisia. J Clin Microbiol 50: 3345–3348.
National AIDS Coordinating Agency (NACA), 2010. The Masa Antiretroviral Therapy Program in Botswana: Patient Enrolment Update. Gaborone, Botswana: NACA.
Nurjadi D, Olalekan AO, Layer F, Shittu AO, Alabi A, Ghebremedhin B, Schaumburg F, Hofmann-Eifler J, Van Genderen PJ, Caumes E, Fleck R, Mockenhaupt FP, Herrmann M, Kern WV, Abdulla S, Grobusch MP, Kremsner PG, Wolz C, Zanger P, 2014. Emergence of trimethoprim resistance gene dfrG in Staphylococcus aureus causing human infection and colonization in sub-Saharan Africa and its import to Europe. J Antimicrob Chemother 69: 2361–2368.
Heysell SK, Shenoi SV, Catterick K, Thomas TA, Friedland G, 2011. Prevalence of methicillin-resistant Staphylococcus aureus nasal carriage among hospitalised patients with tuberculosis in rural Kwazulu-Natal. S Afr Med J 101: 332–334.
Senthilkumar A, Kumar S, Sheagren JN, 2001. Increased incidence of Staphylococcus aureus bacteremia in hospitalized patients with acquired immunodeficiency syndrome. Clin Infect Dis 33: 1412–1416.
Cenizal MJ, Hardy RD, Anderson M, Katz K, Skiest DJ, 2008. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus (MRSA) nasal colonization in HIV-infected ambulatory patients. J Acquir Immune Defic Syndr 48: 567–571.
Kalra L, Camacho F, Whitener CJ, Du P, Miller M, Zalonis C, Julian KG, 2013. Risk of methicillin-resistant Staphylococcus aureus surgical site infection in patients with nasal MRSA colonization. Am J Infect Control 41: 1253–1257.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 57 | 57 | 6 |
Full Text Views | 332 | 123 | 1 |
PDF Downloads | 121 | 51 | 0 |
Staphylococcus aureus is an important cause of morbidity and mortality in children in sub-Saharan Africa (SSA). A major risk factor for staphylococcal infection is S. aureus colonization of the anterior nares. We sought to define risk factors for S. aureus carriage and characterize antimicrobial resistance patterns in children in Botswana. A cross-sectional study was conducted at two clinical sites in southern Botswana. Patients under 18 years of age underwent two nasal swabs and brief interviews, 4 weeks apart. Standard microbiological techniques were used. For persistent carriers, S. aureus was isolated from swabs at both time points, and for intermittent carriers, S. aureus was isolated from only one swab. Poisson regression with robust variance estimator was used to compare prevalence of carriage and the resistance phenotypes. Among 56 enrollees, prevalence of S. aureus colonization was 55% (N = 31), of whom 42% (N = 13) were persistent carriers. Of human immunodeficiency virus–infected children, 64% (N = 9) were carriers. Risk factors for nasal carriage included a history of tuberculosis (prevalence ratio [PR] = 1.60; 95% confidence interval [CI] = 1.02, 2.51; P = 0.040) and closer proximity to health care (PR = 0.89; 95% CI = 0.80, 0.99; P = 0.048). Prior pneumonia was more common among persistent rather than intermittent carriers (PR = 2.64; 95% CI = 1.64, 4.23; P < 0.001). Methicillin-resistant S. aureus (MRSA) prevalence was 13%. Of isolates tested, 16% were resistant to three or more drugs (N = 7/44). In summary, children in southern Botswana are frequently colonized with S. aureus. Antibiotic resistance, especially MRSA, is also widespread. Antibiotic recommendations for treatment of staphylococcal infections in SSA should take cognizance of these resistance patterns.
Financial support: This publication was made possible through core services and support from the Penn Center for AIDS Research (CFAR), an NIH-funded program (P30 AI 045008) and benefitted from funding from the Children's Hospital of Philadelphia Research Institute (to Andrew P. Steenhoff).
Authors' addresses: Michael J. A. Reid, Department of Medicine, University of California San Francisco Medical Center, San Francisco, CA, E-mail: michael.reid2@ucsf.edu. Rebecca S. B. Fischer, Department of Epidemiology, Baylor College of Medicine, Houston, TX, E-mail: rebecca.fischer@bcm.edu. Naledi Mannathoko, School of Medical Sciences, University of Botswana, Gaborone, Botswana, E-mail: nbmannathoko@yahoo.com. Charles Muthoga, Laboratory Sciences, Botswana UPenn Partnership, Gaborone, Botswana, E-mail: muthogac@bup.org.bw. Erin McHugh, Department of Medicine, University of Texas, Houston, TX, E-mail: erin.e.mchugh@uth.tmc.edu. Heather Essigmann and Eric L. Brown, Epidemiology, Human Genetics and Environmental Sciences, University of Texas School of Public Health, Houston, TX, E-mails: heather.t.essigmann@uth.tmc.edu and eric.l.brown@uth.tmc.edu. Andrew P. Steenhoff, Children's Hospital of Philadelphia, Department of Pediatrics, Philadelphia, PA, E-mail: steenhoff@email.chop.edu.
Lowy FD, 1998. Staphylococcus aureus infections. N Engl J Med 339: 520–532.
DeLeo FR, Otto M, Kreiswirth BN, Chambers HF, 2010. Community-associated meticillin-resistant Staphylococcus aureus. Lancet 375: 1557–1568.
Chisti MJ, Tebruegge M, La Vincente S, Graham SM, Duke T, 2009. Pneumonia in severely malnourished children in developing countries: mortality risk, aetiology and validity of WHO clinical signs: a systematic review. Trop Med Int Health 14: 1173–1189.
Sigauque B, Roca A, Mandomando I, Morais L, Quintó L, Sacarlal J, Macete E, Nhamposa T, Machevo S, Aide P, Bassat Q, Bardají A, Nhalungo D, Soriano-Gabarró M, Flannery B, Menendez C, Levine MM, Alonso PL, 2009. Community-acquired bacteremia among children admitted to a rural hospital in Mozambique. Pediatr Infect Dis J 28: 108–113.
Wood SM, Shah SS, Bafana M, Ratner AJ, Meaney PA, Malefho KC, Steenhoff AP, 2009. Epidemiology of methicillin-resistant Staphylococcus aureus bacteremia in Gaborone, Botswana. Infect Control Hosp Epidemiol 30: 782–785.
Cotton MF, Wasserman E, Smit J, Whitelaw A, Zar HJ, 2008. High incidence of antimicrobial resistant organisms including extended spectrum beta-lactamase producing Enterobacteriaceae and methicillin-resistant Staphylococcus aureus in nasopharyngeal and blood isolates of HIV-infected children from Cape Town, South Africa. BMC Infect Dis 8: 40.
Singh V, Aneja S, 2011. Pneumonia: management in the developing world. Paediatr Respir Rev 12: 52–59.
Naidoo R, Nuttall J, Whitelaw A, Eley B, 2013. Epidemiology of Staphylococcus aureus bacteraemia at a tertiary children's hospital in Cape Town, South Africa. PLoS One 8: e78396.
Preidis GA, McCollum ED, Mwansambo C, Kazembe PN, Schutze GE, Kline MW, 2011. Pneumonia and malnutrition are highly predictive of mortality among African children hospitalized with human immunodeficiency virus infection or exposure in the era of antiretroviral therapy. J Pediatr 159: 484–489.
Ahmed AO, van Belkum A, Fahal AH, Elnor AE, Abougroun ES, VandenBergh MF, Zijlstra EE, Verbrugh HA, 1998. Nasal carriage of Staphylococcus aureus and epidemiology of surgical-site infections in a Sudanese university hospital. J Clin Microbiol 36: 3614–3618.
Kluytmans J, van Belkum A, Verbrugh H, 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10: 505–520.
Truong H, Shah SS, Ludmir J, Twananana EO, Bafana M, Wood SM, Moffat H, Steenhoff AP, 2011. Staphylococcus aureus skin and soft tissue infections at a tertiary hospital in Botswana. S Afr Med J 101: 413–416.
Shet A, Mathema B, Mediavilla JR, Kishii K, Mehandru S, Jeane-Pierre P, Laroche M, Willey BM, Kreiswirth N, Markowitz M, Kreiswirth BN, 2009. Colonization and subsequent skin and soft tissue infection due to methicillin-resistant Staphylococcus aureus in a cohort of otherwise healthy adults infected with HIV type 1. J Infect Dis 200: 88–93.
Miller M, Cespedes C, Bhat M, Vavagiakis P, Klein RS, Lowy FD, 2007. Incidence and persistence of Staphylococcus aureus nasal colonization in a community sample of HIV-infected and -uninfected drug users. Clin Infect Dis 45: 343–346.
National AIDS Coordinating Agency (NACA), 2013. Preliminary Results Botswana AIDS Impact Survey IV. Gaborone, Botswana: Statistics Botswana, 25.
Brown EL, Below JE, Fischer RS, Essigmann HT, Hu H, Huff C, Robinson DA, Petty LE, Aguilar D, Bell GI, Hanis CL, 2015. Genome-wide association study of Staphylococcus aureus carriage in a community-based sample of Mexican-Americans in Starr County, Texas. PLoS One 10: e0142130.
Leung NS, Padgett P, Robinson DA, Brown EL, 2015. Prevalence and behavioural risk factors of Staphylococcus aureus nasal colonization in community-based injection drug users. Epidemiol Infect 143: 2430–2439.
McAllister SK, Albrecht VS, Fosheim GE, Lowery HK, Peters PJ, Gorwitz R, Guest JL, Hageman J, Mindley R, McDougal LK, Rimland D, Limbago B, 2011. Evaluation of the impact of direct plating, broth enrichment, and specimen source on recovery and diversity of methicillin-resistant Staphylococcus aureus isolates among HIV-infected outpatients. J Clin Microbiol 49: 4126–4130.
Clinical Laboratory Standards Institute (CLSI), 2013. Performance Standards for Antimicrobial Susceptibility Testing. Twenty-Third Informational Supplement. CLSI Document M100-S23. Wayne, PA: CLSI.
European Committee on Antimicrobial Susceptibility Testing (EUCAST), 2016. Testing EC on AS. Antimicrobial Susceptibility Testing EUCAST Disk Breakpoint Tables for Interpretation of MICs and Zone Diameters, Version 3.0. Available at: http://www.eucast.org/ast_of_bacteria/. Accessed May 14, 2016.
Nouwen JL, Ott A, Kluytmans-Vandenbergh MF, Boelens HA, Hofman A, van Belkum A, Verbrugh HA, 2004. Predicting the Staphylococcus aureus nasal carrier state: derivation and validation of a “culture rule.” Clin Infect Dis 39: 806–811.
Barros AJ, Hirakata VN, 2003. Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 3: 21.
Coutinho LM, Scazufca M, Menezes PR, 2008. Methods for estimating prevalence ratios in cross-sectional studies. Rev Saude Publica 42: 992–998.
Zou G, 2004. A modified Poisson regression approach to prospective studies with binary data. Am J Epidemiol 159: 702–706.
McNally LM, Jeena PM, Gajee K, Sturm AW, Tomkins AM, Coovadia HM, Goldblatt D, 2006. Lack of association between the nasopharyngeal carriage of Streptococcus pneumoniae and Staphylococcus aureus in HIV-1-infected South African children. J Infect Dis 194: 385–390.
Madhi SA, Adrian P, Kuwanda L, Cutland C, Albrich WC, Klugman KP, 2007. Long-term effect of pneumococcal conjugate vaccine on nasopharyngeal colonization by Streptococcus pneumoniae—and associated interactions with Staphylococcus aureus and Haemophilus influenzae colonization—in HIV-infected and HIV-uninfected children. J Infect Dis 196: 1662–1666.
Bhattacharya SD, Niyogi SK, Bhattacharyya S, Arya BK, Chauhan N, Mandal S, 2012. Associations between potential bacterial pathogens in the nasopharynx of HIV infected children. Indian J Pediatr 79: 1447–1453.
Krcmery V, Sokolova J, Kulkova N, Liskova A, Shahum A, Benca G, 2013. Nasopharyngeal bacterial colonisation in HIV-positive children in Cambodia. Trop Med Int Health 18: 1267–1268.
Zervou FN, Zacharioudakis IM, Ziakas PD, Rich JD, Mylonakis E, 2014. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus colonization in HIV infection: a meta-analysis. Clin Infect Dis 59: 1302–1311.
Korenromp EL, Williams BG, Schmid GP, Dye C, 2009. Clinical prognostic value of RNA viral load and CD4 cell counts during untreated HIV-1 infection: a quantitative review. PLoS One 4: e5950.
Chambers HF, Hartman BJ, Tomasz A, 1985. Increased amounts of a novel penicillin-binding protein in a strain of methicillin-resistant Staphylococcus aureus exposed to nafcillin. J Clin Invest 76: 325–331.
Chambers HF, 1997. Methicillin resistance in staphylococci: molecular and biochemical basis and clinical implications. Clin Microbiol Rev 10: 781–791.
Dien Bard J, Hindler JA, Gold HS, Limbago B, 2014. Rationale for eliminating Staphylococcus breakpoints for beta-lactam agents other than penicillin, oxacillin or cefoxitin, and ceftaroline. Clin Infect Dis 58: 1287–1296.
Schaumburg F, Alabi AS, Peters G, Becker K, 2014. New epidemiology of Staphylococcus aureus infection in Africa. Clin Microbiol Infect 20: 589–596.
Maalej SM, Rhimi FM, Fines M, Mnif B, Leclercq R, Hammami A, 2012. Analysis of borderline oxacillin-resistant Staphylococcus aureus (BORSA) strains isolated in Tunisia. J Clin Microbiol 50: 3345–3348.
National AIDS Coordinating Agency (NACA), 2010. The Masa Antiretroviral Therapy Program in Botswana: Patient Enrolment Update. Gaborone, Botswana: NACA.
Nurjadi D, Olalekan AO, Layer F, Shittu AO, Alabi A, Ghebremedhin B, Schaumburg F, Hofmann-Eifler J, Van Genderen PJ, Caumes E, Fleck R, Mockenhaupt FP, Herrmann M, Kern WV, Abdulla S, Grobusch MP, Kremsner PG, Wolz C, Zanger P, 2014. Emergence of trimethoprim resistance gene dfrG in Staphylococcus aureus causing human infection and colonization in sub-Saharan Africa and its import to Europe. J Antimicrob Chemother 69: 2361–2368.
Heysell SK, Shenoi SV, Catterick K, Thomas TA, Friedland G, 2011. Prevalence of methicillin-resistant Staphylococcus aureus nasal carriage among hospitalised patients with tuberculosis in rural Kwazulu-Natal. S Afr Med J 101: 332–334.
Senthilkumar A, Kumar S, Sheagren JN, 2001. Increased incidence of Staphylococcus aureus bacteremia in hospitalized patients with acquired immunodeficiency syndrome. Clin Infect Dis 33: 1412–1416.
Cenizal MJ, Hardy RD, Anderson M, Katz K, Skiest DJ, 2008. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus (MRSA) nasal colonization in HIV-infected ambulatory patients. J Acquir Immune Defic Syndr 48: 567–571.
Kalra L, Camacho F, Whitener CJ, Du P, Miller M, Zalonis C, Julian KG, 2013. Risk of methicillin-resistant Staphylococcus aureus surgical site infection in patients with nasal MRSA colonization. Am J Infect Control 41: 1253–1257.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 57 | 57 | 6 |
Full Text Views | 332 | 123 | 1 |
PDF Downloads | 121 | 51 | 0 |