Typhi research by Dr. Andre Hattingh done in Democratic Republic of Congo : Typhoid fever is a type of enteric fever, along with paratyphoid fever. The cause is the bacterium Salmonella Typhi, also known as Salmonella enterica serotype Typhi, growing in the intestines and blood. Typhoid is spread by eating or drinking food or water contaminated with the feces of an infected person.

                                      03 February 2014

Prevalence of Salmonella typhi and parathyphi infected children:
A Hopital du Cinquantenaire de Kisangani based study.

Dr. J. Andre Hattingh MD. Ph.D. DTM&H

Medical Director

Hopital du Cinquantenaire de Kisangani Democratic Republic of Congo



The purpose of this study was to find out the prevalence and antibiotic sensitivity pattern of Salmonella typhi and paratyphi isolated from children presenting with fever at Hopital du Cinquantenaire de Kisangani in Oriental province Democratic Republic of Congo.

A total of 7500 blood samples collected  from in and outpatients at Hopital du Cinquantenaire de Kisangani for culture during one year period (January 2013 to January 2014) were included in this study. Out of total, 247 (3.3%) were positive for S. typhi and paratyphi A. Of the total positive, 207 (84%) were S.typhi and  40 (16%) were S.paratyphi A. The growth positive rate in two genders (M 53.2% and F46.8%) was not significant (P>0.05). Over two-third of cases were clustered in the age group 0-16 years. The occurrence of infections was 64% more common between the months of February to October. S.typhi was found to be more sensitive to Cefotaxime (100%)  followed by Ceftriaxone (96%)  Ofloxacin (90%) Cotrimoxazole (89.3%)  and Chloramphenicol (87.6%) and was least sensitive to Amoxycillin (64.6%) followed by Ciprofloxacin (77.9%)

S.Paratyphi was also found to be most sensitive to Cefotaxime (100%) followed by Ceftriaxone (97.9%), Cotrimoxazole (97.1%) and Chloramphenicol (92.5%) and was least sensitive to Amoxycillin (15%) followed by Ciprofloxacin (51.3%) and Ofloxacin (70.3%)



Enteric fever is an important public health problem in many underdeveloped and developing countries1 including Kisangani in the Democratic Republic of Congo. (Democratic Republic of Congo). Though it occurs also in developed countries, the incidence and case fatality rate is very low.3 The global incidence is estimated to be 21 million with 700 000 deaths each year primarily in South east Asia, Africa and Latin America4 attributed to rapid population growth and unplanned urbanization, inadequate and improper waste disposal, lack of potable water supply. Outbreaks are more common in summer season5 affecting mainly children.6 Infected and healthy carriers are the source of infection and “four f’s”          ( food, fingers, flies, and faeces)play an important role in the spread of the disease.

Enteric fever is predominantly caused by S.typhi followed by S. Paratyphi A. 6   Though antimicrobial therapy markedly reduces the morbidity and mortality, emergence of resistance to first line antibiotics poses a challenge in its management. Resistance to Chloramphenicol, “gold standard of therapy” since its introduction in 1948,8  appeared in 1970 leading to many outbreaks in Countries in Latin America and Asia.9 It then resulted into multi drug resistance (MDR: resistant to Ampicillin, Cotrimoxazole and Chloramhenical) in 1989.10  Fluoroquinolones were the drug of choice for MDR S.typhi in Asia for the past decade.11  However, emergence of resistance even to these drugs has become a major setback in the management. Moreover, third generation cephalosporin’s used as alternative agents are also becoming less effective.12  However, there are evidence of re-emergence of sensitivity of S. Typhi to Chloramphenicol as reported in Lancet 1999, 353:1241-213 and observed by me at Hopital du Cinquantenaire de Kisangani in Oriental province Democratic Republic of Congo, therefore it is essential to reappraise the antibiotic sensitivity pattern of the isolates periodically.

Enteric fever (Typhoid fever) in Kisangani is more common during the months of February to October. As the disease is most commonly seen in children in our Hospital, this paper reports the prevalence and antibiogram of S. Typhi and paratyphi A and isolates, isolated from mainly children presenting with fever.


A total of 7500 children (neonates and children aged 0 up to 16 years) presenting with fever at Hopital du Cinquantenaire de Kisangani in Kisangani, Oriental province Democratic Republic of Congo in one year period January 2013 to January 2014 were included in this study. Blood samples collected by aseptic venipuncture were subjected to bacteriological culture (1ml of blood was put in 10ml brain heart infusion broth) and incubated at 370 C over night followed by sub-culture on MacConkey agar. Growth negative culture was continued incubation for 5 days sub-culturing in between at intervals of 48, 72 and 96 hours. Growth negative even after 120 hours incubation were regarded as negative. The non-lactose fermenting colonies MacConkey agar resembling Salmonella were subjected for serotyping using polyvalent and monovalent antisera (Denka-Seiken Company LTD Japan).

S.typhi and paratyphi A isolates were subjected to antimicrobial susceptibility testing following Kirby-Bauer’s disk diffusion technique using Muller Hinton Agar. Antibiotic discs used in this study included Amoxycillin (10mcg), Chloramphenicol (30mcg), Cotrimoxazole (25mcg), Ciprofloxacin (5mcg), Ofloxacin (5mcg), Ceftriaxone (5mcg), and Cefotaxime (5mcg). The sensitivity and/or resistance results of the tested isolates were recorded following the instructions of the disc manufacturer.


Fig.-1: Distribution of Salmonella positive cases per month at Hopital du Cinquantenaire de Kisangani, Oriental province Democratic Republic of Congo.


Of the total 7500 blood samples cultured 247 (3.3%) were positive for S.typhi and paratyphi A . Out of the total positive samples 207 (84%) were S.typhi and 40 (16%) S. Paratyphi A. S. Paratyphi B and C were not isolated. The overall growth positive rate was relatively higher in male (53.2%) compared to female (46.8%) children but the difference was not significant statistically (P.0.05) (Table1). Similar trend in growth positivity of S.typhi (M: 55% and F: 45%) was observed in both sexes. Over two third of growth positive cases were seen in age-group of 1-10 years. The occurrence of enteric fever was higher in tropical summer months. (Fig-1)

S. Typhi was found to be most sensitive to Cefotaxime (100%) followed by Ceftriaxone (98.9%), Ofloxacin(90%) Cotrimoxazole (89.3%)  and Chloramphenicol (87.6%) and was least sensitive to Amoxycillin (64.6%) followed by Ciprofloxacin (77.9%). (Table-3)



Enteric fever is common in developing countriesincluding the Democratic Republic of Congo (Democratic Republic of Congo). It is attributed to rapid population growth and unplanned urbanization, inadequate and improper waste disposal, and lack of potable water supply4 . Emergence of drug resistance in the organism pose a great challenge.15 Physicians, therefore, should always be aware of the antibiotic sensitivity/resistance profile of the organism in a given community16  for the correct and rational use of antibiotics.17 

In this study, children aged 1-10 years were mostly effected (over two thirds of the growth positive cases). However, Ansari et al18  have reported two third of the cases to be in the age group 4-9 years. A definate difference in our mean age group at Hopital du Cinquantenaire de Kisangani of 1 to 10 years old. Enteric fever appears to be rare among under one year of age20, five cases (2.1%) were found in this study. Interestingly, S. Typhi was isolated also from a one-month old infant. Reed et al21  also reported similar findings and postulated that the bacteria might have transmitted through vertical route.

Though males had marginally higher incidence, it was not significant (male to female ratio 1.1:1). A slightly different male to female ratio has been reported by Bhattarai et al (1.2:1)14  and Ansari et al (1.3:1)18  The male preponderance seen could be due to their relatively higher outdoor activities exposing them to the source of infection.

This appeared to be due to contamination of drinking water and environment with fecal mater. The open drains next to the streets in Kisangani become flooded by rainwater mixed with bad smelling safety tank overflow and faeces from residents that uses the “bush” as toilets.

The incidence of S.typhi and  S.paratyphi seen in this study was similar to findings reported by Mubeena et al from Pakistan. In the contrary, Mella et al 2 have reported a lower percentage of S. Typi cases from Nepal. This difference could be due to the inclusion of adult and elderly population by them.

S.typhi was most sensitive to Cefotaxime followed by Ceftriaxone, Ofloxacin, Cotrimoxazole and Chloramphenicol in this study. This was in agreement to previous findings 14,18  . However much lower sensitivity (69.1%) has also been reported. 26  A very small percentage (1.1%) of S.typhi was resistant to Ceftriaxone and was in agreement with the findings reported from Pakistan.12,25


In this study, sensitivity to Chloramphenicol was (92%). This observation was similar to the findings reported by other investigators from Nepal.26  Bhatia et al in India have reported 96.0% and 100% sensitivity of S. Typhi and S. Paratyphi respectively. Nair et al 15  have shown a decreasing trend in resistance to Chloramphenicol (50% in 1995 to 12.5% in 2003). Malla et al2 have also reported a decreasing resistance pattern to Chloramphenicol (30.0% in 2002 to 5.0% in 2004). On the other hand, Mubeena et al25  in Pakistan found a very low sensitivity to Chloramphenicol (27%). Low sensitivity (60%) has also been reported in eastern Nepal27 .

In this study, it is worth noting of higher sensitivity to Cotrimoxazole (+93%). This was higher than those reported earlier (64.3% by Bhattarai et el 14  and 74.4% by Mubeena et al25 )The resistance pattern of the isolates to Cotrimoxazole during recent years is decreasing (from 80.0% in 1995 to 37.7% in 2003 in India15  ) and ( from 30.0% in 2002 to 5% in 2004 in Nepal2 ).

Two-third of S.typhi were sensitive to Amoxicillin. It was similar to the findings of Bhattarai et al14 . On the contrary, Rauniar et al27  observed a higher sensitivity rate to this drug (80%). On the other hand, another study done in India22  showed very low sensitivity (40%).

S.paratyphi was found to be most sensitive to Cefotaxime, followed by Ceftriaxone, Cotrimoxazole and Chloramphenicol. Fifteen percent of S. Paratyphi was sensitive to Amoxycillin.

Although the culture positive rate for S.typhi and S.paratyphi A was only 2.0% of total blood culture samples collected from children presenting with fever, it still indicates the major health importance of this disease in the Oriental province Democratic Republic of Congo. Despite the use of only seven antibiotics for sensitivity testing, these findings help to make known the present status of Enteric fever among children from Kisangani. It is advisable to do sensitivity tests of Cefixime, the recommended drug in the treatment of Enteric fever. Considering the changing drug sensitivity pattern (sensitive to resistance and vice-versa) it is advisable to do continuous evaluation of sensitivity-resistance pattern of isolates as to make rational use of antibiotics in the management of enteric fever cases in future.



  1. Shanahan PM, Jesudason MV, Thomson CJ, Amyes SG.

Molecular analysis and identification of antibiotic resistance

genes in clinical isolates of  Salmonella typhi from India. J

Clin Microbiol 1998; 36: 1595-600.

  1. Malla S, Kansakar P, Serichantalergs, Rahman M, Basnet S.

Epidemiology of typhoid and paratyphi fever in Kathmandu:

two years study and trends of antimicrobial resistance. J Nepal

Med Assoc 2005; 44: 18-22.

  1. Ackers ML, Puhr ND, Tauxe RV, Mintz ED. Laboratory-based

surveillance of  Salmonella serotype typhi infections in the

United States: antimicrobial resistence on the rise.  J Amer

Med Assoc 2000; 283: 2668-73.

  1. Edelman R, Levine MM. Summery of an international

workshop on typhoid fever. Rev Infect Dis1986; 8: 329-49

  1. Fjaerli HO, Heger B, Gundersen SG, Hoet T, Espinoza R.

Outbreak of typhoid in family. Tidsskr nor Leageforen 1993;

113: 3022-4.

  1. Ratish KC, Chandrashekhar MR, Nagesha CN. An outbreak

of multidrug resistant typhoid fever in Bangalore.  Indian J

Pediar 1995; 62: 445-8.

  1. Old DC, Threlfal EJ. Salmonella In: Topley and Wilson’s

Microbiology and Microbial Infections, 9


 edition, volume

2 (Systemic Bacteriology), Arnold, London 1998, 969-97.

  1. Bha t i a JK, Ma thur  AD,  Aror a  MM.  Re eme rgenc e  of

chloramphenicol sensitivity in enteric fever. Med J Armed

Forces India 2007; 63: 212-14.

  1. Olarte J, Galindo E. S. typhi resistant to chloramphenicol,

ampicillin and other antimicrobial agents: strains isolated in

extensive typhoid fever epidemic in Mexico.  Antimicrob

Agents Chemother 1973; 4: 597-601.

  1. Jesudason MV, Malathy B, John TJ. Trend of increasing levels

of MIC of ciprofloxacin to S. typhi. Indian J Med Res 1996;

103: 247-9.

  1. Gulati PD, Saxena SN, Gupta PS, Chuttani HK. Changing

pattern of typhoid fever. Amer J Med 1968; 45: 544-8.

  1. Jamil B, Lashari I, Bhatti S, Hasan RS. Enteric fever in adult

p a t i e n t s :   c l i n i c a l   f e a t u r e s ,   o u t c ome   a n d   a n t i b i o t i c s

s u s c e p t i b i l i t y   p a t t e r n s .   I n f e c t  Di s   J   P a k i s t a n

2004; 13: 68-72.

  1. Sood S, Kapil A, Das B, Jain Y, Kabra SK. Reemergence of

c h l o r amp h e n i c o l   s e n s i t i v e   S a lmo n e l l a   t y p h i.   L a n c e t

1999; 353: 1241-2.

  1. Bhattarai PM, Bista KP, Dhakwa JR et al. A clinical profile

of enteric fever at Kanti Children’s Hospital. J Nepal Paediatr

Soc 2003; 21: 50-3.

  1. Na i r L, Suda r s ana   J .  Changing  s ens i t ivi ty pa t t e rn of

Salmonella typhi in Calicut. Calicut Med J 2004; 2: 141-4.

  1. Oreskovic NM, Sembrano EU. Repeat urine cultures in

children who are admitted with urinary tract infections.

Pediatr 2007; 119: 325-9.

  1. Jones RN, Thornsberry C. Cefotaxime: a review of in vitro

antimicrobial properties and spectrum of activity. Rev Infect

Dis 1982; 4: 5300-15.

  1. Ansari I, Adhikari N, Pandey R, Dangal MM, Karanjit R.

Enteric fever: is ciprofloxacin failing? J Nepal Paediatr Soc

2002; 20: 6-16.

  1. Prakash P, Mishra OP, Singh AK, Gulati AK, Nath G.

Evaluation of nested PCR in diagnosis of typhoid fever.  J

Clin Microbiol 2005; 43: 431-2.m

  1. Bhutta ZA. Typhoid Fever. In: Nelson Textbook of Pediatrics;

18th ed, Philadelphia, WB Saunders 2007; 1186-91.

  1. Reed RP, Klugman KP. Neonatal typhoid fever. Pediatr Infect

Dis J 1994; 13: 774-7.

  1. Khan M, Coovadia YM, Connolly C, Sturm AW. Influence

o f   s e x   o n   c l i n i c a l   f e a t u r e s ,   l a b o r a t o r y   f i n d i n g s   a n d

complications of typhoid fever.  Amer J Trop Med Hyg

1999; 61: 41-6.

  1. Rai SK, Shrestha HG, Nakanishi M et al. Hookworm infection

recorded at an university teaching hospital in Kathmandu,

Nepal over one decade period.  Japanese J Trop Med Hyg

1997; 25: 81-4.

  1. Adhikari RK, Rai SK, Pokhrel BM, Khadka JB. Bacterial

study of drinking water of Kathmandu Valley.  J Inst Med

(Nepal) 1986; 8: 313-6.

  1. Mubeena RS, Saleem AK, Ameena RS. Prevalence of enteric

fever in Karachi. Infect Dis J Pakistan 2006: 15: 103-5.

  1. Sharma N, Koju R, Karmacharya B et al. Typhoid fever in

Dh u l i k h e l  Ho s p i t a l ,  Ne p a l .   K a t hma n d u  Un i v  Me d   J

2003; 2: 188-92.

  1. Rauniar GP, Das BP, Baral DD, Nagarani MA. Treatment

pattern of typhoid fever at a tertiary care teaching hospital in

Eastern Nepal. J Nepal Med Assoc 2000; 39: 218-21.

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