Open Access

Prevalence of enteric infections among hospitalized patients in two referral hospitals in Ghana

  • R. Akuffo1, 2, 3Email author,
  • G. Armah1,
  • M. Clemens2, 3,
  • K. C. Kronmann4, 8,
  • A. H. Jones2, 3,
  • P. Agbenohevi5,
  • K. Sagoe6,
  • N. Puplampu4,
  • N. Talla Nzussouo7,
  • W. Ampofo1,
  • K. Koram1,
  • C. Duplessis4 and
  • E. Dueger2, 3, 7
BMC Research Notes201710:292

https://doi.org/10.1186/s13104-017-2621-x

Received: 12 May 2016

Accepted: 12 July 2017

Published: 17 July 2017

Abstract

Background

Diarrhea is an important cause of morbidity and mortality worldwide. In Africa and Ghana in particular, it is estimated to contribute directly to 19 and 25% of pediatric mortality among children under 5 years, respectively.

Methods

Surveillance for hospitalized acute diarrheal illness was initiated in November 2010 through October 2012 in a referral hospital in southern Ghana, and a teaching hospital in northern Ghana. Consenting hospitalized patients who met a standardized case definition for acute diarrheal illness provided demographic and epidemiologic data. Stool samples were collected and tested by culture for bacteria and by enzyme immunoassays for a panel of viruses and parasites.

Results

A total of 429 patients were enrolled; 216 (50.3%) were under 5 years, and 221 (51.5%) were females. Stool samples were received from 153 patients. Culture isolates included Shigella sp., Salmonella spp., Plesiomonas sp. and Vibrio cholerae. Of 147 samples tested for viruses, 41 (27.9%) were positive for rotaviruses, 11 (7.5%) for astroviruses, 10 (6.8%) for noroviruses, and 8 (5.4%) for adenoviruses. Of 116 samples tested for parasitic infections; 4 (3.4%) were positive for Cryptosporidium sp. and 3 (2.6%) for Giardia lamblia. Of the enrolled patients, 78.8% had taken antibiotics prior to sample collection.

Conclusions

Diarrheal pathogens were identified across all ages, however, predominantly (81%) in the children under 5 years of age. This study also detected high antibiotic use which has the potential of increasing antibiotic resistance. The most common enteric pathogen detected (49.4%) was rotavirus.

Keywords

Prevalence Enteric Infections Pathogens Diarrhea Surveillance Hospitalized

Background

Diarrheal disease, caused by a wide variety of viral, bacterial and parasitic pathogens, is a common cause of morbidity, hospitalization and mortality worldwide and occurs among people of all ages [1, 2]. It is the second leading cause of death among children under 5 years and is estimated to have caused 0.578 million pediatric deaths (0.448–0.750 million; 9.2%, 7.1–11.9) worldwide [36] with most deaths occurring in children in developing (low and middle income) countries. In Africa, diarrhea is estimated to cause 19% of childhood (<5 years) deaths [3] and accounts for 25% of pediatric mortality in Ghanaian children <5 years of age [7].

Some recent studies have attempted to describe the burden, epidemiology and etiological fraction of diarrhea in developing countries [8, 9] including Ghana [10, 11]. Most attributable cases of moderate-to-severe diarrhea identified in these studies included rotavirus, norovirus, astrovirus, Cryptosporidium parvum, Campylobacter spp., Vibrio cholerae, Aeromonas spp., enterotoxigenic Escherichia coli producing heat-stable toxin (ST-ETEC; with or without co-expression of heat-labile enterotoxin), and Shigella spp. [810]. While this development is encouraging, there is still limited data on diarrhea among hospitalized patients across all ages in Ghana.

In this work, we present results regarding the epidemiology and prevalence of acute diarrheal illness in Ghana based on a hospitalized study group.

Methods

Surveillance for hospitalized acute diarrheal illness was initiated in November 2010 until October 2012, in two public referral hospitals in Ghana; 37 Military Hospital (37MH) in the Greater Accra Region (Southern Ghana), and the Tamale Teaching Hospital (TTH) in the Northern Region of Ghana (Additional file 1).

A case of hospitalized acute diarrheal illness was defined as a hospitalized adult or child aged 31 days or older with the passage of three or more watery or loose stools in a 24-h period or more but less than 14 days in duration. This criteria also included hospitalized patients aged 31 days and above with two loose or liquid stools in a 24-h period or more, prior to admission and at least one of the following symptoms: history of fever (with current illness), dysentery, abdominal pains/cramps, nausea and vomiting, within a 14 day period. Suspected cases were identified from the admissions log book on the infectious disease wards of participating hospitals based on chief complaint of diarrhea reported at the time of admission. Hospitalized patients who met the case definition for diarrheal illness or their parents or legal guardians (in the case of children) were invited to participate in the study. Patients who developed diarrhea after admission were not included in the study.

Demographic and epidemiological data were obtained by the administration of a structured questionnaire using personal digital assistants (PDAs). Data was also collected on antibiotic use prior to hospital admission and prior to sample collection. Hospital folders of consented patients were also monitored for outcome information including the weekly monitoring of antibiotic administration (if any) after specimen collection.

Stool samples were collected from enrolled patients within 24 h of admission and stored at 2–8 °C at the study sites and transported within 24 h of sample collection to NMIMR at same temperature, using cool box with ice packs (without stool transport medium such as Cary Blair) for stool culture as well as virus and parasite enzyme immunoassay (EIA) testing respectively. Samples for bacteria culture were plated on MacConkey, Salmonella/Shigella and TCBS agar plates and cultured for 24–48 h at 37 °C. Apart from Vibrio cholerae, isolates were identified using biochemical methods and confirmed with the API-20E bacterial identification test strip from BioMerieuxInc©, France. Antimicrobial susceptibility testing (AST) was performed on isolates using disc diffusion method, with the cut-off inhibition zone diameter values for resistance, intermediate and susceptible determined using the performance standards for antimicrobial susceptibility testing twenty-first informational supplement [12].

AST to trimethoprim/sulphamethoxazole, ampicillin, ciprofloxacin, amikacin, gentamycin, cephalothin, ampicillin-sulbactam, nalidixic acid, imipenem, cefotaxime, chloramphenicol, tetracycline, and aztreonam was conducted for Salmonella sp. and Plesiomonas sp. respectively. Wampole™ Giardia II, E. histolytica and Cryptosporidium test kits, from Techlabs, USA, were used for the parasite enzyme immunoassays (EIA). The IDEIA ™Rotavirus, Adenovirus, Norovirus and Astrovirus test kits (OxoidLtd, UK) were used for the virus EIAs. If a sample was insufficient for all testing, lab tests were prioritized in the following order: stool culture, viral EIA and parasite EIA, respectively.

All statistical tests were conducted at a 95% confidence level.

Results

A total of 429 hospitalized patients who met the case definition for acute diarrheal illness provided consent and assent (for children) for study inclusion (Table 1). Age range of enrolled patients was 1 month to 95 years; 216 (50.3%) were under 5 years, and 221 (51.5%) were females (Table 2). Symptoms reported by participants include vomiting, history of fever, abdominal cramps, nausea and dysentery in 347 (80.9%), 300 (69.9%), 156 (36.4%), 78 (18.2%) and 57 (13.3%).
Table 1

Distribution of enrolled participants and samples received from study sites

Study site

Enrolled, n (%)

Samples received, n (%)

TTH

141 (32.9)

44 (28.8)

37MH

288 (67.1)

109 (71.2)

Total

429

153

TTH Tamale Teaching Hospital, 37MH 37 Military Hospital

Table 2

Demographic and clinical characteristics of enrolled ADI cases

Characteristic

Subgroups

Enrolled (N = 429)

Age group

31 days to <1 years

98 (22.8)

 

1 to <5 years

118 (27.5)

 

5 to <18 years

21 (4.9)

 

18 to <65 years

171 (39.9)

 

65 years+

21 (4.9)

 

Male

200 (46.6)

Sex

Female

221 (51.5)

 

Missing

8 (1.9)

 

Antibiotic use prior to admission

49 (11.4)

Antibiotic use

Antibiotic use prior to sample collection

338 (78.8)

Outcomea

Discharge

395 (96.6)

 

Death

12 (2.9%)

 

Unknown/missing

22 (5.4)

Data is represented in N (%)

aOutcome data available for 409 participants

Duration of diarrheal symptoms experienced by the enrolled participants is presented in Table 3, of which majority (90.2%) were within 0–5 days. In addition, majority of the enrolled patients 232 (54.0%) were hospitalized for a duration of 1–3 days while 110 (25.7%), 37 (8.7%), and 50 (11.6%) patients were hospitalized for periods of 4–6 days, 7–9 days and >10 days respectively.
Table 3

Duration of diarrheal symptoms among enrolled study participants (N = 429); Nov 2010–Sep 2012

Duration of diarrheal symptoms (days)

Number of participants

0–1

98 (22.8)

2–3

185 (43.2)

4–5

104 (24.2)

6–7

35 (8.2)

8–9

3 (0.7)

10–12

4 (0.9)

Data is represented in N (%)

Forty-nine (11.4%) of the enrolled cases reported antibiotic use prior to hospital admission; the indication for antibiotic use prior to hospital admission was however unclear. Furthermore, antibiotics, including ciprofloxacin (41.5%), metronidazole (22.8%), cefuroxime (17.8%) and ceftriaxone (16.0%), were administered to 338 (78.8%) of the consented patients prior to specimen collection.

Data on outcome of hospitalization was available for 409 (95.3%) of the enrolled patients; 395 (96.6%) were discharged, and 12 (2.9%) died. Of the patients who died, 5 (41.7%), 3 (25%), 3 (25%), and 1 (9.1%) had outcome diagnoses (the diagnosis given to the participant closest in time to their death) of gastroenteritis, pneumonia, malaria, and congestive cardiac failure respectively. The mean age of the patients who died was 19 years (range 5 months to 52 years). Four (33.3%) of those who died submitted stool samples for processing. Of these, three tested positive for specific enteric pathogens; rotavirus [2] and adenoviruses [1].

A total of 153 (35.7%) stool samples (Table 1) were collected from the enrolled patients, of which 99 (64.7%) were from children under 5 years. All 153 samples were cultured for bacterial isolates. Viral EIA was performed on 147 (96.1%) of the samples; six of the samples had insufficient quantity after culture. Parasite EIA was conducted on 116 (75.8%) samples; the remaining had insufficient quantity of sample following viral EIA testing.

Bacterial pathogens were isolated from 6 (3.9%) of the 153 stool samples cultured. These included one Shigella spp., one Vibrio cholerae, two Salmonella sp., and two Plesiomonas shigelloides. Although Escherichia coli was identified in 62 (40.5%) of the samples tested, this study did not determine whether the E. coli observed were diarrheagenic.

The Salmonella sp. isolates were resistant to nalidixic acid, chloramphenicol, tetracycline, ampicillin, ciprofloxacin, and aztreonam antibiotics while the Plesiomonas sp. were resistant to trimethoprim/sulphamethoxazole, ampicillin, amikacin, gentamycin, cephalothin, nalidixic acid, imipenem, tetracycline and aztreonam (Table 4). ASTs were not conducted for the Vibrio cholerae and Shigella sp.
Table 4

Antimicrobial susceptibility testing results for Salmonella sp. and Plesiomonas sp.

Antimicrobial agent

Disk conten (μg)

Inhibition zone diameter for different pathogens (mm)b

Salmonella sp. 1

Salmonella sp. 2

Plesiomonas sp. 1

Plesiomonas sp. 2

Amikacin

30

18

17

12a

12a

Ampicillin

10

8a

9a

8a

8a

Ampicillin–sulbactam

10/10

18

18

17

19

Aztreonam

30

14a

12a

13a

14a

Cefotaxime

30

28

27

30

29

Cephalothin

30

20

21

11a

12a

Chloramphenicol

30

9a

9a

15

16

Ciprofloxacin

5

12a

11a

24

23

Gentamycin

10

14

13

8a

8a

Imipenem

10

26

24

17a

15a

Nalidixic acid

30

10a

9a

9a

8a

Tetracycline

30

8a

8a

10a

9a

Trimethoprim/sulfamethoxazole

23.75

18

19

8a

8a

aResistant

bCut-off inhibition zone diameter values determined using the performance standards for antimicrobial susceptibility testing twenty-first informational supplement for CLSI [12]

Of the 147 samples tested by viral EIA, 41 (27.9%) were positive for rotaviruses, 11 (7.5%) for astroviruses, 10 (6.8%) for noroviruses and 8 (5.4%) for adenoviruses. Two of the rotavirus positive samples also tested positive for noroviruses while one sample was positive for both astrovirus and norovirus. In addition, one of the rotavirus positive samples was also positive by culture to Shigella sp. and Plesiomonas shigelliodes. Furthermore, our study identified peaks in rotavirus infection during January–March of the years 2011 and 2012 respectively (Fig. 1). Of the 116 samples tested for parasitic infections; 4 (3.4%) were positive for Cryptosporidium sp. and 3 (2.6%) for Giardia lamblia respectively. The majority (81%) of enteric pathogens detected were among children under 5 years (Table 5). No significant difference was observed between the enrolled participants who provided sample and those who did not provide sample.
Fig. 1

Monthly distribution of ADI enrolled cases (lower panel, n = 429) and pathogens detected from samples tested (upper panel, n = 83); Nov 2010–Oct 2012

Table 5

Age distribution of stool pathogens detected (N = 83); Nov 2010–Sep 2012

Stool pathogens

Frequency

Age groupa

31 days to <1 years

1–5 years

>5 years

Rotavirus

41

17 (41.5)

22 (53.7)

2 (4.9)

Norovirus

10

3 (30.0)

2 (20.0)

5 (50.0)

Astrovirus

11

4 (36.4)

2 (18.2)

5 (45.5)

Adenovirus

8

4 (50.0)

3 (37.5)

1 (12.5)

Cryptosporidium

4

3 (75.0)

0 (0)

1 (25.0)

Giardia

3

2 (66.7)

0 (0)

1 (33.3)

Salmonella sp.

2

1 (50.0)

1 (50.0)

0 (0)

Plesiomonas sp.

2

2 (100.0)

0 (0)

0 (0)

Vibrio Cholerae

1

0 (0)

0 (0)

1 (100.0)

Shigella sp.

1

1 (100.0)

0 (0)

0 (0)

Total

83

37 (44.6)

30 (36.1)

16 (19.3)

aData is represented in N (%)

Discussion

Most (84.3%) of the enteric pathogens identified in our study were viruses of which rotavirus constituted the majority (58.6%) (Table 5). Rotavirus is known to be the most common cause of severe acute, watery diarrhea in children under 5 years of age in industrialized and developing parts of the world [13], with over 80% of deaths attributable to it, and occurring in the poorest nations of South Asia and sub-Saharan Africa [14, 15].

Multiple studies in Ghana among children <5 years of age confirm the prominent role of rotavirus in pediatric gastroenteritis [10, 11, 1619]. Our study identified peaks in rotavirus infection during January–March of the years 2011 and 2012 respectively (Fig. 1) while earlier diarrhea surveillance studies in other regions of Ghana identified diarrhea peaks in October–March [2225].

Two rotavirus vaccines are available for use and are recommended by the World Health Organization (WHO) for inclusion in the routine immunization program of nations [20] and has been part of Ghana’s expanded program of immunization (EPI) since late April 2012 [21].

Recent studies in Ghana have reported decline in hospitalization due to severe diarrhea after the introduction of the rotavirus vaccines and we anticipate that ongoing surveillance for rotavirus disease in Ghana will reveal a further decrease in the absolute prevalence of rotavirus associated diarrheal disease and hospitalization [21].

Although almost 50% of samples tested positive for pathogenic viruses in this study, the percentage of cases with identifiable bacterial and parasitic pathogens (~4%) was relatively small compared to other studies which recorded up to 20–30% identifiable bacterial and parasitic pathogens [4, 7, 2631]. However, studies on the etiologies of acute diarrhea in non-hospitalized patients in Ghana unveiled a 5% prevalence rate of bacterial and parasitic pathogens [19] very similar to what we have observed in this study. The overall low bacterial pathogen detection rate in our study is likely multi-factorial.

With the exception of suspected Shigella (dysentery) and cholera, the WHO strongly discourages the use of antibiotics in the treatment of diarrhea since indiscriminate antibiotic use increases resistance to antibiotics of many disease-causing organisms [32, 33]. Previous studies in Ghana have reported the emergence of antibiotic resistance of diarrheal pathogens [34, 35]. As a result, the high use of antibiotics for treatment of diarrhea in Ghana should be of concern to all (Table 5).

Giardia lamblia, Entamoeba histolytica, and Cryptosporidium parvum are the major parasitic organisms causing childhood diarrhea in developing countries [28]. These have been estimated to be associated with 15–20 and 2–5% of diarrhea cases in developing and developed countries respectively [30]. We identified Giardia and Cryptosporidium in 2.6 and 3.4% of participants respectively. The observed detection rates in our study was however lower than the 11.4% intestinal parasites incidence reported by Nkrumah [30] with Giardia being the most common (89.0%), and the 8.2% recorded for Cryptosporidium in children <2 years by Opintan et al. in Ghana [35].

Nkrumah et al. used direct microscopy of smears in saline to identify parasites while Opintan et al. used polymerase chain reaction to identify the Cryptosporidium. Both studies included outpatients and were focused on children under 5 years whereas our study focused on inpatients and included patients across all ages. The widespread antibiotic use encompassing metronidazole, prior to sample collection, may have contributed to the low parasite yield observed in our study.

Recent data on diarrhea in developing countries call for a paradigm shift for future studies on diarrhea in these countries, including Ghana. While some studies have previously suggested that certain diarrheal pathogens such as enterotoxigenic Escherichia coli and rotaviruses predominate in developing countries, with others being more common globally and in developed areas [36], available data suggests that there is no evidence that any particular pathogen or type of pathogen is associated with persistent diarrhea in children under the age of six in low and middle income countries [4]. There is therefore a need for future diarrheal surveillance in developing countries and Ghana in particular, to ensure that a wide range of diarrheagenic pathogens are tested.

Conclusions

Diarrheal pathogens identified among hospitalized patients in the Greater Accra and Northern regions of Ghana occurred across all ages and included bacteria, parasites and viruses. In view of the high antibiotic use observed in this study, antibiotic susceptibility testing should be integrated into surveillance programs to dictate the appropriate antibiograms which are always in flux.

Limitations

  • This study was not population based, so only represents infection prevalence among hospitalized cases who provided stool samples, not burden of diseases in general population.

  • A large proportion of enrolled cases did not provide samples mainly because they were discharged within a day after admission, before the surveillance team could obtain sample from them. This may have biased available data on duration of hospitalization.

  • Stool transport medium (such as Cary Blair) was not used and hence may have likely contributed to the low bacterial isolation detected.

  • This study did not look for Campylobacter and diarrheagenic E. coli in the samples collected.

  • The high antibiotic use observed in this study may have had an effect on the bacterial yield observed.

Abbreviations

ADI: 

acute diarrheal infections

EIA: 

enzyme immunoassay

GHS: 

The Ghana Health Service

NAMRU-3: 

US Naval Medical Research Unit No. 3

CDC: 

US Centers for Disease Control and Prevention

WHO: 

World Health Organization

EPI: 

expanded program of immunization

Declarations

Authors' contributions

Conceived and designed the study: ED, GA, KK, WA, KK. Conducted the study: ED, GA, KS, PA, NP, RA. Analyzed the data: RA. Wrote the manuscript: RA, GA, MC, K, AJ, PA, KS, NP, NT, W, KK, CD, ED. All authors read and approved the final manuscript.

Acknowledgements

The authors wish to thank the USA Centers for Disease Control and Prevention and the Global Emerging Infections Surveillance and Response System (GEIS) Operations, a division of the Armed Forces Health Surveillance Center (AFHSC), for funding to undertake this study, the administrations, staff and surveillance staff of 37th Military Hospital, Tamale teaching hospital for their dedication to the project. We also acknowledge the Director and staff of Noguchi Memorial Institute for Medical Research (NMIMR), the Director General of GHS, the Public Health Division of GHS, and the Director General of Ghana Armed Forces Medical Services for logistical and technical support. The staff of the Electron Microscopy Department of NMIMR are appreciated for their role in sample processing. We also wish to thank staff and officer in charge of the Ghana Detachment of the US Naval Medical Research Unit No. 3 (NAMRU-3), Cairo for their support with sample processing, data management and project coordination.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

Data for this manuscript as well as information on all materials used in this study are available upon request from the corresponding author. Data for this manuscript shall made available in a publicly available and accessible data repository after publishing of manuscript.

Disclaimer

The findings and conclusions in this report are those of the authors and do not necessarily represent the official policy of the U.S. Government, the U.S. Centers for Disease Control and Prevention, the Department of Defense or the Department of the Navy. The study protocol number 908 entitled Integrated Hospital-Based Infectious Disease Surveillance in the Greater Accra and Northern Regions, Ghana, was reviewed and approved by the institutional review board of the U.S. Naval Medical Research Unit No. 3, in compliance with all federal regulations governing the protection of human subjects.

Ethics approval and Consent to Participate statement

The study protocol was approved by the Institutional Review Boards at U.S. Naval Medical Research Unit No. 3 (NAMRU3.2009.0008), the U.S. Centers for Disease Control and Prevention (5654), Noguchi Memorial Institute for Medical Research (NMIMR-IRB CPN 029/08-09), and the Ghana Health Service of the Republic of Ghana (GHS-ERC-04/2/09) in compliance with all applicable federal regulations governing the protection of human subjects. Informed consent to participate in the study was obtained from all participants (or their parent or legal guardian in the case of children under 18 years). Additionally, any child whose age is greater than or equal to 8 years and less than 18 years was given an opportunity to sign the child assent portion of the consent form, prior to enrolment.

Funding

This project was funded by the US Centers for Disease Control and Prevention and the Global Emerging Infections Surveillance and Response System (GEIS) Operations, a division of the Armed Forces Health Surveillance Center (AFHSC).

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Authors’ Affiliations

(1)
Noguchi Memorial Institute for Medical Research
(2)
Global Disease Detection & Response Program (GDDRP), U.S. Naval Medical Research Unit No. 3 (NAMRU-3)
(3)
Global Disease Detection (GDD) Egypt Regional Center, U.S. Naval Medical Research Unit No. 3
(4)
U.S. Naval Medical Research Unit No. 3, Ghana Detachment
(5)
37 Military Hospital
(6)
Tamale Teaching Hospital
(7)
U.S. Centers for Disease Control and Prevention
(8)
Uniformed Services University of the Health Sciences

References

  1. Boschi-Pinto C, Velebit L, Shibuya K. Estimating child mortality due to diarrhoea in developing countries. Bull World Health Organ. 2008;86:710–7.View ArticlePubMedPubMed CentralGoogle Scholar
  2. World Health Organization N. The Global Burden of Disease: 2004 update. Update. http://www.who.int/healthinfo/global_burden_disease/2004_report_update/en/index.html. Accessed 10 Jan 2016.
  3. O’Reilly CE, Jaron P, Ochieng B, Nyaguara A, Tate JE, Parsons MB, et al. Risk factors for death among children less than 5 years old hospitalized with diarrhea in rural Western Kenya, 2005–2007: a cohort study. PLoS Med. 2012;9:e1001256.View ArticlePubMedPubMed CentralGoogle Scholar
  4. Abba K, Sinfield R, Hart CA, Garner P. Pathogens associated with persistent diarrhoea in children in low and middle income countries: systematic review. BMC Infect Dis. 2009;9:88.View ArticlePubMedPubMed CentralGoogle Scholar
  5. Wilson ME. Diarrhea in nontravelers: risk and etiology. Clin Infect Dis. 2005;41(Suppl 8):S541–6.View ArticlePubMedGoogle Scholar
  6. Liu L, Oza S, Hogan D, Perin J, Rudan I, Lawn JE, Cousens S, Mathers C, Black RE. Global, regional, and national causes of child mortality in 2000–13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet. 2015;385(9965):371–9. doi:https://doi.org/10.1016/S0140-6736(14)61698-6.View ArticleGoogle Scholar
  7. Binka E, Vermund SH, Armah GE. Rotavirus as a cause of diarrhea among children under 5 years of age in urban Ghana: prevalence and serotypes/genotypes. Pediatr Infect Dis J. 2011;30(8):718–20.View ArticlePubMed CentralGoogle Scholar
  8. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sur D, Breiman RF, Faruque ASG, Zaidi AKM, Saha D, Alonso PL, Tamboura B, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O’Reilly CE, Mintz ED, Muhsen K, Sommerfelt H, Robins-Browne RM. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case–control study. Lancet. 2013;382:209–22.View ArticlePubMedGoogle Scholar
  9. Platts-Mills JA, Babji S, Bodhidatta L, Gratz J, Haque R, Havt A, et al. Pathogen-specific burdens of community diarrhoea in developing countries: a multisite birth cohort study (MAL-ED). Lancet Glob Heal. 2015;3(9):564–75.View ArticleGoogle Scholar
  10. Krumkamp R, Sarpong N, Schwarz NG, Adelkofer J, Loag W, Eibach D, et al. Gastrointestinal infections and diarrheal disease in Ghanaian infants and children: an outpatient case–control study. PLoS Negl Trop Dis. 2015;9(3):1–14.View ArticleGoogle Scholar
  11. Leva A, Eibach D, Krumkamp R, Käsmaier J, Rubbenstroth D, Adu-Sarkodie Y, et al. Diagnostic performance of the Luminex xTAG gastrointestinal pathogens panel to detect rotavirus in Ghanaian children with and without diarrhoea. Virol J. 2016;13(1):132.View ArticlePubMedPubMed CentralGoogle Scholar
  12. Cockerill F, Wikler M, Bush K, Al E. Performance standards for antimicrobial susceptibility testing twenty-first informational supplement, vol. 1, issue no 21. Clinical and Laboratory Standards Institute, Wayne. 2010.Google Scholar
  13. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380:2095–128.View ArticlePubMedGoogle Scholar
  14. Mbuh FA, Armah GE, Omilabu SA, Ahmad AA, Umoh JU. Molecular epidemiology of group A human rotaviruses in North West region, Cameroon. Pan Afr Med J. 2012;12:108.PubMedPubMed CentralGoogle Scholar
  15. Nordgren J, Nitiema LW, Sharma S, Ouermi D, Traore AS, Simpore J, et al. Emergence of unusual G6P[6] rotaviruses in children, Burkina Faso, 2009–2010. Emerg Infect Dis. 2012;18:589–97.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Hori H, Akpedonu P, Armah G, Aryeetey M, Yartey J, Kamiya H, et al. Enteric pathogens in severe forms of acute gastroenteritis in Ghanaian children. Acta Paediatr Jpn. 1996;38:672–6.View ArticlePubMedGoogle Scholar
  17. Asmah RH, Green J, Armah GE, Gallimore CI, Gray JJ, Iturriza-Gómara M, et al. Rotavirus G and P genotypes in rural Ghana. J Clin Microbiol. 2001;39:1981–4.View ArticlePubMedPubMed CentralGoogle Scholar
  18. Group TNRR. Incidence and risk factors of paediatric rotavirus diarrhoea in northern Ghana. Trop Med Int Health. 2003;8(9):840–6.View ArticleGoogle Scholar
  19. Reither K, Ignatius R, Weitzel T, Seidu-Korkor A, Anyidoho L, Saad E, et al. Acute childhood diarrhoea in northern Ghana: epidemiological, clinical and microbiological characteristics. BMC Infect Dis. 2007;7:104.View ArticlePubMedPubMed CentralGoogle Scholar
  20. Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, Rodriguez Z, et al. Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med. 2006;354:23–33.View ArticlePubMedGoogle Scholar
  21. Enweronu-Laryea CC, Boamah I, Sifah E, Diamenu SK, Armah G. Decline in severe diarrhea hospitalizations after the introduction of rotavirus vaccination in Ghana: a prevalence study. BMC Infect Dis. 2014;14(1):431.View ArticlePubMedPubMed CentralGoogle Scholar
  22. Ali-Shtayeh MS, Hamdan AH, Shaheen SF, Abu-Zeid I, Faidy YR. Prevalence and seasonal fluctuations of intestinal parasitic infections in the Nablus area, West Bank of Jordan. Ann Trop Med Parasitol. 1989;83:67–72.View ArticlePubMedGoogle Scholar
  23. Armah GE, Mingle JA, Dodoo AK, Anyanful A, Antwi R, Commey J, et al. Seasonality of rotavirus infection in Ghana. Ann Trop Paediatr. 1994;14:223–9.View ArticlePubMedGoogle Scholar
  24. Black RE, Brown KH, Becker S, Yunus M. Longitudinal studies of infectious diseases and physical growth of children in rural Bangladesh: patterns of morbidity. Am J Epidemiol. 1982;115:305–14. doi:https://doi.org/10.1093/oxfordjournals.aje.a113307.View ArticleGoogle Scholar
  25. Mertens TE, Wijenayake R, Pinto MR, Peiris JS, Wijesundera MD, Eriyagama NB, et al. Microbiological agents associated with childhood diarrhoea in the dry zone of Sri Lanka. Trop Med Parasitol. 1990;41:115–20.PubMedGoogle Scholar
  26. Kosek M, Bern C, Guerrant RL. The global burden of diarrhoeal disease, as estimated from studies published between 1992 and 2000. Bull World Health Organ. 2003;81:197–204.PubMedPubMed CentralGoogle Scholar
  27. Makobe CK, Sang WK, Kikuvi G, Kariuki S. Molecular characterization of virulence factors in diarrhoeagenic Escherichia coli isolates from children in Nairobi, Kenya. J Infect Dev Ctries. 2012;6:598–604.View ArticlePubMedGoogle Scholar
  28. El-mohammady H, Mansour A, Shaheen HI, Henien NH, Motawea S, Rafaat I, et al. Original article increase in the detection rate of viral and parasitic enteric pathogens among Egyptian children with acute diarrhea. J Infect Dev Ctries. 2012;6(11):774–81.View ArticlePubMedGoogle Scholar
  29. Yilgwan C, Okolo S. Prevalence of diarrhea disease and risk factors in Jos University Teaching Hospital. Nigeria. Ann Afr Med. 2012;11:217.View ArticlePubMedGoogle Scholar
  30. Nkrumah B, Nguah SB. Giardia lamblia: a major parasitic cause of childhood diarrhoea in patients attending a district hospital in Ghana. Parasit Vectors. 2011;4(1):163.View ArticlePubMedPubMed CentralGoogle Scholar
  31. Bern C, Martines J, de Zoysa I, Glass RI. The magnitude of the global problem of diarrhoeal disease: a 10-year update. Bull World Health Organ. 1992;70:705–14.PubMedPubMed CentralGoogle Scholar
  32. World Health Organization. The Management and prevention of diarrhoea: practical guidelines. Geneva: World Health Organization; 1993.Google Scholar
  33. Laxminarayan R, Bhutta ZA. Antimicrobial resistance—a threat to neonate survival. Lancet. 2016;4:e676–7.PubMedGoogle Scholar
  34. Djie-Maletz A, Reither K, Danour S, Anyidoho L, Saad E, Danikuu F, et al. High rate of resistance to locally used antibiotics among enteric bacteria from children in Northern Ghana. J Antimicrob Chemother. 2008;61:1315–8.View ArticlePubMedGoogle Scholar
  35. Opintan JA, Newman MJ, Ayeh-Kumi PF, Affrim R, Gepi-Attee R, Sevilleja JEAD, et al. Pediatric diarrhea in Southern Ghana: etiology and association with intestinal inflammation and malnutrition. Am J Trop Med Hyg. 2010;83:936–43.View ArticlePubMedPubMed CentralGoogle Scholar
  36. Guerrant RL, Hughes JM, Lima NL, Crane J. Diarrhea in developed and developing countries: magnitude, special settings, and etiologies. Rev Infect Dis US. 1990;12(1):S41–50.View ArticleGoogle Scholar

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