|Year : 2019 | Volume
| Issue : 2 | Page : 556-563
An outbreak of cutaneous leishmaniasis among a displaced population in North Sudan: Review of cases
Amel Abdalrhim Sulaiman1, Wadie Mohammed Elmadhoun2, Sufian Khalid Noor3, Sarra Osman Bushara3, Ahmed O Almobarak4, Heitham Awadalla5, Elmoubashar Farag6, Mohamed H Ahmed7
1 Community Medicine Specialist, Department of Public Health - MOH, Qassim Region-Saudi Arabia, Saudi Arabia
2 Department of Pathology and Microbiology, College of Medicine- Nile Valley University, Khartoum, Sudan
3 Department of Internal Medicine, College of Medicine- Nile Valley University, Khartoum, Sudan
4 Department of Pathology, Faculty of Medicine, University of Medical Sciences and Technology, Khartoum, Sudan
5 Department of Community Medicine, Faculty of Medicine, University of Khartoum, Sudan
6 Deparment of Public Health, Doha, Qatar
7 Department of Medicine and HIV Metabolic Clinic, Milton Keynes University Hospital NHS Foundation Trust, Eaglestone, Milton Keynes, Buckinghamshire, UK
|Date of Web Publication||28-Feb-2019|
Dr. Mohamed H Ahmed
Department of Medicine and HIV Metabolic Clinic, Milton Keynes University Hospital NHS Foundation Trust, Eaglestone, Milton Keynes, Buckinghamshire
Source of Support: None, Conflict of Interest: None
Background: Human cutaneous leishmaniasis (CL) is an endemic disease in many parts of Sudan. Objective: To document an outbreak of CL among internally displaced people (IDP) in north Sudan. Methods: A household survey was conducted in the rural region of New Manasir, at El Damer Locality in north Sudan during the year 2013. All villagers were screened for recent and old skin lesions in addition to other urgent medical problems. Written consent was obtained from each participant before data collection. A pretested, interviewer-administered questionnaire was used to collect the socio-demographic and clinical characteristics of participants. The diagnosis of CL was based on clinical findings and/or identification of the amastigotes on skin smears. Results: Out of the 1,236 individuals enrolled in this survey, 688 were diagnosed as cases of CL, giving an infection rate of 55.7%. Children constituted 244 (35.5%) of infected cases. Majority of skin lesions were found in the Extremities 524 (76.2%). The average duration of skin lesions was 3.6 months (±1.6). Conclusion: This outbreak among IDPs affected a large proportion of inhabitants of the newly established villages in north Sudan. Preventive measures might have help control such outbreaks.
Keywords: Cutaneous leishmaniasis, displaced population, North Sudan, outbreak, prevalence
|How to cite this article:|
Sulaiman AA, Elmadhoun WM, Noor SK, Bushara SO, Almobarak AO, Awadalla H, Farag E, Ahmed MH. An outbreak of cutaneous leishmaniasis among a displaced population in North Sudan: Review of cases. J Family Med Prim Care 2019;8:556-63
|How to cite this URL:|
Sulaiman AA, Elmadhoun WM, Noor SK, Bushara SO, Almobarak AO, Awadalla H, Farag E, Ahmed MH. An outbreak of cutaneous leishmaniasis among a displaced population in North Sudan: Review of cases. J Family Med Prim Care [serial online] 2019 [cited 2019 Nov 15];8:556-63. Available from: http://www.jfmpc.com/text.asp?2019/8/2/556/253047
| Highlights|| |
- Cutaneous Leishmaniasis (CL) is one of the neglected tropical diseases, distributed in wide geographical areas worldwide
- Sudan was hit by CL outbreaks many times with the presence of sporadic cases from time to time mainly in the Eastern part of the country
- This outbreak of CL has a major significance due to it, s occurrence in a displaced population who were settled in anew green area (New Manasir Villages)
- The low immunity of displaced population in addition to the presence of vector resulting in a hight prevalent of CL (55.7%)
- An aggressive appearance of some cases of CL reported during this outbreak.
| Introduction|| |
Leishmanias is is a protozoan parasitic disease transmitted by sand fly species. The disease has four main clinical forms: cutaneous leishmaniasis (CL), mucocutaneous leishmaniasis (ML), visceral leishmaniasis (VL), and the post-kala-azar dermal leishmaniasis (PKDL).,, Cutaneous leishmaniasis is estimated to cause the ninth largest disease burden in terms of morbidity and mortality among infectious diseases and is largely neglected in tropical and sub-tropical countries., Cutaneous leishmaniasis is considered as a major public health problem worldwide and associated with an increase in both morbidity and mortality. The disease also causes serious economic loss and impedes socio-economic development in many countries, especially in Africa, Indian Subcontinent, Eastern and Southern Mediterranean Regions and countries of the Middle East.,,
Several contributing factors play an important role in increasing CL disease, which includes inadequate vector and reservoir control, urbanization, ecological changes, natural disasters, population movement, poor sanitation, and human behavioral risk factors.,, All of these factors can lead to favor epidemic, emergence, and spread of CL.
In Sudan, CL is caused by L. major, zymodeme LON-1. The vector is Phlebotomus papatasi and the animal reservoir host is probably the Nile rat Arvicanthis niloticus. Leishmaniasis is an endemic disease spread over wide geographical areas in the country. CL occurs in a fluctuating pattern in the country mainly in the west, central, and northern parts of Sudan.
The first known outbreak of cutaneous leishmaniasis in Khartoum involved about 10,000 recorded cases. The peak of the outbreak was in September 1986. The disease was widespread all over the province, mainly along the banks of the River Nile. People of both sexes, all age groups, different ethnic origins, and all socioeconomic classes were equally affected, suggesting that this epidemic was a new occurrence among a non-immune population.
Possible contributory factors were mass population movement from known endemic areas of CL in Sudan, migration, displacement, high population densities of sand flies, and an increase in the rodent population.
Cutaneous leishmaniasis outbreak usually occurred in the poorest regions and the poorest populations. It has adverse effects on the patients, skin ulcers causing serious disability, disfiguring, and permanent scarring after healing.
This survey aimed to document the infection rate of CL, and to describe a new focus of CL in northern Sudan from epidemiological aspects of the CL disease including; age, gender, wound site, duration of lesions, seasonality of the disease. The findings of this survey, therefore, may update the available information about the disease in northern Sudan and may be considered a baseline for future control of CL especially in River Nile State (RNS).
| Methods|| |
This survey was conducted in Village Two in New Manasir area located in El Damer Locality, River Nile State, Sudan in a period from 8th May through to 23rd May 2013.
As a result of the construction of the Merowe hydroelectric dam in north Sudan, over 60,000 people were displaced from their origin homes in Old Manasir during the years 2006 through 2009. Manasir tribe were the most affected population because their lands and houses were demolished due to Make Lake of the constructed dam. The Government of Sudan gave compensation and new resettlement places for the affected people. Alternative settlement places in RNS were arranged for them viz. Albuhaira and Alfida in Abu Hamed locality and the New Manasir in El Damer Locality. A large proportion of the displaced people settled in the New Manasir area that included six villages in RNS. In these villages, big agricultural schemes were established and every household was given the land of (5 acres) to make their living. Infrastructure services were provided e.g., a well-equipped primary health care centers, local markets and community centers for each village. Each village is composed of 24 residence squares, every square contains 40 houses. Though the farm was adjacent to houses in these villages, most of the villagers have their animals including cattle, donkeys, and dogs living within houses or a temporary shelter immediately outside their homes, making frequent and close exposure to animals. The villages are located on a surface land, the water is held permanently throughout the year from River Nile through a big channel. The local climate is desert-like, cold in winter, dry, and hot in the summer.
Study design and data collection
This survey was carried out in the most inhabited village (village 2) in New Manasir. Trained medical students from Faculty of Medicine, Nile Valley University collected the data from the household. Two physicians, in addition to a dermatologist and a microbiologist, were among the survey team. A pretested questionnaire was used that included 20 questions divided into 3 sections; section one composed of demographic and epidemiological data, section two were the duration, site, size, shape and other characteristics of skin lesion and section three inquired about the perception of patients about the methods of prevention.
The diagnosis of CL was made by clinical observations and identification of Leishman Donovan (LD) bodies on skin smears.
Examination of skin smears
Microscopic examination: Lesions were cleaned with ethanol and punctured at the margins of the lesion with a sterile lancet. Smears were made from the exudating material, air dried and fixed in methanol. Then they were stained with Giemsa's stain for examination by light microscopy.
The data generated were coded, entered, validated and analyzed using SPSS, version 21, for Windows (SPSS Inc., Chicago, IL). Chi-squared test was used to compare the association between proportions. A P value of ≤0.05 was considered statistically significant.
Permission was obtained from the local community leaders before commencing the field work and consent was obtained from every participant/guardian before starting data collection. The following information was given during data collection to ensure they had the information needed to make an informed choice: the participation was optional; there would be no penalty for refusal to participate; a complete description of the aims of the study; potential benefits and risks, assurance of confidentiality of any information given and test results. Any other requested additional information was provided by data collectors. During the outbreak, the main concern of health authorities was to manage cases and prevent transmission. Patients who had active lesion were transferred to the nearest PHCC for further management. This survey was augmented by a campaign to raise the awareness of the community. A senior dermatologist was available during the time of survey to provide consultation and management. A drug of Leshimanol provided free of charge for those who had active lesions during the survey.
Ethical approval was obtained from the Ethical Committee of Nile Valley University and the State Ministry of Health.
| Results|| |
Characteristics of the study population
A total of 1,236 population were randomly selected from the household survey in Village Two, New Manasir – RNS, 2013 year. There were 709 (57.4%) males and 527 (42.68%) females in the study group. Most study participants 938 (75.9%) were newly settled in new Manasir area in a period from 2007 to 2008 and the rest in the succeeding years. One-third of the study population 365 (29.5%) were illiterate. More than half of the study population 668 (54.0%) lived in a family with 4-7 family members. Participants had a different occupation; housewives were 322 (26.1%), students 309 (25.0%), and farmers were 307 (24.8%), more details about the socio-demographic characteristics were displayed in [Table 1].
|Table 1: Characteristics of the surveyed population, NewManasir- RNS, 2013 (n=1,236)|
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Prevalence of cutaneous leishmaniasis
The prevalence rate of CL among the population in New Manasir area was 55.7% (688/1236), [Table 2]. The distribution of the infected cases by clusters in the village were shown on the [Map 1] and [Map 2]. Children under 15 years old were the most affected age group 383 (55.6%), while 305 cases (44.3%) reported in adults [Table 2]. The male to female ratio was approximately 1:1.
|Table 2: Clinical characteristics of Cutaneous Leishmaniasis patients, New Manasir- RNS, 2013 (n=688)|
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Prevalence of CL infection according to the sex and age
It was observed that the highest outbreak of disease with 244 (35.5%) had occurred in children mainly the age group of 6–15 years [Table 2]. A significant statistical correlation was found between the age group and gender of the infected people (P, 0.00), males, were more affected than females, 128 (52.5%) vs. 116 (47.5%) in the same age group (6–15 years). But in the adult age group ranging from 16 to 60 + years old, we noticed the prevalence of the disease was slightly higher among female than male [Figure 1].
|Figure 1: Distribution of the CL infected cases in relation to the age group and sex, New Manasir- RNS, 2013 (n = 688)|
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Data obtained from questionnaires and physical examination of study population showed a prevalence of Papuloplaque 52.2%, Nodule and ulcer 45.2%, and scar 2.6%. Most patients 539 (78.3%) had no history of traveling to endemic areas.
Multiple symptoms were noticed in 50.4% of patients in addition to other symptoms like; Itching 37.6%, Pain 4.3%, and Discharge 2.8% [Table 2].
A positive reaction to the leishmanin skin test (LST) was observed in 12.2% (84 individuals, 21 females, and 63 males) of volunteers.
The distribution of lesions in the patients' body parts was varied as is shown in [Table 2], the majority of the lesions 524 (76.2%) were found in the extremities (legs and hands). In relation to the distribution of lesions site and age groups, children group, shown the highest percentage in all sites of the lesions in comparison to the adult's group. However, site of lesions in extremities (hands and legs) remained high percent in both adults and children age groups. In children age groups, skin lesions in trunk represent the highest percent (95.2%), while in extremities the lowest percent (52.2%). This is opposite of the adult's age groups where the highest percent of the skin lesion in extremities (47.8%) and lowest in head and neck (25%) [Table 3].
|Table 3: Distribution of the CL infected cases in relation to age group and site of the lesion(s), New Manasir- RNS, 2013 (n=688)|
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Duration of skin lesions was ranged between 1 and 6 month in most of the cases (66.4%), an average was 3.6 (±1.6) months. Healing occurred in 78.2% of patients, while in a few cases (13.2%) the cured individuals experienced a new secondary lesion(s). More than half of the patients 409 (59.4%) were used different types of local mediation; the mixture of stuff and Tar, Herbs and Cauterization, 31.5%, 20.9%, and 7%, respectively. [Table 2] A significant statistical correlation was found between the level of education and the use of local medication (P, 0.01).
The rate of CL infection in relation to certain social and environmental factors; the maximum cases 485 (70.5%) had been infected in the winter season. A significant statistical correlation was found between the patients' gender and occupation as risk (P, 0.00).
Knowledge of the surveyed population
Only 295 (42.9%) out of 688 of the study population correctly recognized the vector to be sand fly, 369 (53.6%) did not know the mode of transmission, and 24 (3.5%) had misbeliefs about the mode of transmission [Table 2].
The perception of patients about the prevention of CL was varied, half of them 51.5% (354) did not know the prevention methods, and few of them knew the correct method for control of the diseases; those who knew the chemical barriers were 194 (28.2%) and physical barriers were 52 (7.5%). No statistical correlation had been approved between the educational level and patients' knowledge regarding the prevention methods of CL [Table 2].
| Discussion|| |
Cutaneous leishmaniasis causes a public health problem in several countries. Its prevalence was under-estimated due to under-reporting, misdiagnosis, or non-diagnosis.,
In Sudan, it occurs sporadically throughout the years but for the last decade, it showed extension in its geographical distribution, due to some interlinking factors such as the state of immunity of infected humans and changes in the population of reservoir and vector due to changes in the environment. The climatic fluctuations affect the population of sand flies and reservoir hosts. The unusual weather may also cause a shift in the factors affecting transmission thus resulting in outbreaks of the disease. The migration and movement of people from endemic to non-endemic areas also increases the risk of infection because of ecological and environmental changes.,,
This study of importance due to many reasons; first, it following the residence of the displaced population in new settlement (New Mansir area) which is previously uninhabited. Second, the study population had no history of C L in their old place (old Manasir).
The present survey revealed that the outbreak of CL occurred among the population who moved from dry areas to a new Manasir area where many agriculture schemes and irrigations are available. This environmental changes may encourage sand flies activity.
The prevalence rate of infection was determined by clinical examination in almost 90% of the resident population. Considering that, the prevalence rate of 55.7% reported in this study seems to be high, and could reflect the occurrence of an almost sever outbreak of CL in the area. This finding was higher than the prevalence of CL in Morocco (42%), Pakistan (40%), and Yemen (18.8%).,,
In the current study, it was observed that the highest outbreak of disease with 35.5% had occurred in children mainly in the age group of 6–15 years. This finding was similar to the study conducted in Iran where the highest outbreak of scars was observed in the age group of 10–14 years. The highest infection is statistically significant (P, 0.00) among males aged group of (6–15), but not in females of the same age group. This may be due to the increased activity of males aged than females during this age. However, the reasons for the highly significant and higher prevalence rate in younger age is probably due to the fact that they have poorly developed an immune system. They cannot prevent themselves from bites of sand flies and do not have enough knowledge of defending themselves. Similar results and discussion were observed in different studies.,
The results indicate that the outbreak of CL was different in gender among adults group. Women were more affected than men, this could be probably due to in rural areas women involve in agricultural activities as same as the men and are equally exposed to the infected bites. Also, due to the geographical site where water stream flows all year and the near distances between populations' houses the agriculture where sand flies can be found.,,
In this outbreak, the majority of skin lesions were seen on the external extremities (hands and legs) of the body. The findings are compatible with the results of studies conducted in many endemic areas of disease., However, in children less than 15 years old the common location of lesions was in the trunk of the body, this could be due to sleeping out of the covered area or house yards without using bed-nets during the summer. Furthermore, the extremities without any clothing can easily expose to the bites of sand flies.
This survey has identified that the outbreak of CL lesions in most of the cases has occurred in the winter. In fact, Sudan is located in the tropical area where the temperature is lowered only during the winter season and then it gives a chance for sand flies to breed. In contrast, in Western Iran most cases were infected during Autumn. This may suggest the peak of breading of sand flies can extend from Autumn till Summer. The main risk factor associated with the increase in the incidence of CL is the presence of sand flies. Therefore, the control of the vectors is a key factor in stopping and reducing the transmission of the disease, especially in the domestic and peridomestic context.
In this survey, we found that the patients' knowledge about prevention methods was poor, few of them were aware of the correct method for control of CL (chemical or barrier methods). In fact use of the chemical method in the prevention of CL has a role to control the disease, but in Sudan, sand flies may have developed resistance to insecticides. This can be attributed in part to intensive use of insecticides by malaria control programmes and in agricultural practice, especially in northern parts of the country.,,
So for reduction of CL cases, the use of barrier methods (chemical and physical) is important to prevent bites, environmental management to prevent the proliferation of insects; avoiding stagnant water, elimination of waste dumps, improve housing conditions and raise the community awareness.
Limitations of the study
This study is not without limitations. Some of the cases had already healed lesions, therefore, a microbiological diagnosis was not possible. Another drawback was the lack of (antigenic and genomic) characterization of the Leishmania strains, in order to establish epidemiological links with other future outbreaks. Moreover, no field study in vector insects or potential reservoirs in order to identify the possible focus so as to facilitate the effectiveness of control measures.
| Conclusion|| |
The findings of this study identified that via the movement of displaced population to New Manasir, many risk factors might have been created, that were associated with epidemics of CL. Such precipitating factors included environmental conditions, individual and behavioral changes and the arrival of the non-immune population to an endemic area. These factors could activate epidemics of old foci and induce new emerging foci.
We believe that essential measures should have been taken to contain the epidemics such as proper surveillance of diseases in the new settlement areas, the introduction of environmental measures to prevent the proliferation of sand flies, identification of the main reservoir, and personal protection systems.
Special thanks to the General Director of the State Ministry of Health for his help in transportation and drugs provision. We thanks also the local community leaders for their facilitation. We are grateful to the 5th batch medical students in the Faculty of Medicine and Health Sciences, Nile Valley University for their help in data collection. Also, our thanks extend to the statistician particularly Ms. Hiba Ahmed who help in data entry and analysis.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Murray HW, Berman JD, Davies CR, Saravia NG. Advances in leishmaniasis. Lancet 2005;366:1561-77.
Babiker AM, Ravagnan S, Fusaro A, Hassan MM, Bakheit SM, Mukhtar MM, et al.
Concomitant infection with leishmaniadonovani and L. major in single ulcers of cutaneous leishmaniasis patients from Sudan. J Trop Med 2014;2014:170859.
Torres-Guerrero E, Quintanilla-Cedillo MR, Ruiz-Esmenjaud J, Arenas R. Leishmaniasis: A review F1000Res 2017;6:750.
Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, et al.
Leishmaniasis worldwide and global estimates of its incidence. PLoS One 2012;7:e35671.
Rhajaoui M. Les leishmanioseshumaines au Maroc: Unediversité nosogéographique. Pathol Biol 2009;10:226-9.
World Health Organization [WHO]: Cutaneous leishmaniasis control in selected countries of the WHO Eastern Mediterranean and African Regions. Report of an interregional network meeting. Casablanca, Morocco, June 23-24, 2014. Available from: http://www.emro.who.int/health-topics/leishmaniasis/index.html
. [Last accessed on 2017 Dec 18].
Aflatoonian MR, Sharifi I, Abbasi R, Ranjbar L. To evaluate the cost of prevention on incidence of cutaneous leishmaniasis due to earthquake in Bam. Iran J Epidemiol 2010;6:32-8.
Daszak P, Cunningham AA, Hyatt AD. Anthropogenic environmental changes and the emergence of infectious diseases in wildlife. Acta Trop 2001;78:103-16.
Desjeux P. The increase in risk factors for the leishmaniasis worldwide. Trans Roy Soc Trop Med Hyg 2001;95:239-43.
Macpherson CNL. Human behavior and the epidemiology of parasitic zoonoses. Int J Parasitol 2005;35:1319-31.
Zijlstra EE, El-Hassan AM. Leishmaniasis in Sudan. Visceral leishmaniasis. Trans R Soc Trop Med Hyg 2001;95(Suppl 1):27-58.
El-Hassan AM, Zijlstra EE. Leishmaniasis in Sudan. Cutaneous leishmaniasis. Trans R Soc Trop Med Hyg 2001;95(Suppl 1):1-17.
Kweku MA, Odoom A, Puplampu N, Desewu K, Nuako GK, Gyan B, et al.
An outbreak of suspected cutaneous leishmaniasis in Ghana: Lessons learnt and preparation for future outbreaks. Glob Health Action 2011;4. doi: 10.3402/gha.v4i0.5527.
Escobar MA, Martinez F, Scott S, Palma GI. American Cutaneous and mucocutaneous leishmaniasis (tegumentary): A diagnostic challenge. Trop Dr 1992;22:69-78.
Soomro FR, Pathan GM, Abbasi P, Bajaj D, Bhatti NS, Hussain J, et al.
Asurvey of cutaneous leishmaniasis at village Gaibi Dero, District Larkana, Sindh, Pakistan. Gomal J Med Sci 2009;7:2.
Metcalf CJ, Walter KS, Wesolowski A, Buckee CO, Shevliakova E, Tatem AJ, et al.
Identifying climate drivers of infectious disease dynamics: Recent advances and challenges ahead. Proc R Soc 2017;284:20170901.
Hakkour M, Hmamouch A, El Alem MM, Rhalem A, Amarir F, Touzani M, et al.
New epidemiological aspects of visceral and cutaneous leishmaniasis in Taza, Morocco. Parasit Vectors 2016;9:612.
Asmaa Q, AL-Shamerii S, Al-Tag M, AL-Shamerii A, Osman BH. Parasitological and biochemical studies on cutaneous leishmaniasis in Shara'b District, Taiz, Yemen. Ann Clin Microbiol Antimicrob 2017;16:47.
Saghafipour A, Rassi Y, Abai MR, Oshaghi MA, Farzinnia B, Mostafavi R, et al
. Outbreak of zoonotic cutaneous leishmaniasis: A report. Arch Hyg Sci 2013;2:48-54.
Silva Sde O, Wu AA, Evans DA, Vieira LQ, Melo MN. Leishmania sp. isolated from human cases of cutaneous leishmanias is in Brazil characterized as Leishmania major-like. Acta Trop 2009;112:239-48.
Surendran SN, Kajatheepan A, Ramasamy R. Socio-environmental factors and sand fly prevalence in Delft Island, Sri Lanka: Implications for leishmaniasis vector control. J Vect Borne Dis 2007;44:65-8.
Hanafi Majd AA, Yaghoobi Ershadi MR, Zamani G, Barzekar A, Jafari R, Poor Abazari GR. Epidemiologic aspects of cutaneaus Leishmaniasis Hajiabad, Hormozgan, Iran, 2003. J HormozganUniv Med Sci 2006;10:64-70.
Sharifi I, Zamani F, Aflatoonian MR, Fekri AR. An epidemic of cutaneous leishmaniasis in Baft District in Kerman Province and its probable causative risk factors. Iran J Epidemiol 2008;4:53-8.
Hamidi Farahani R, Tajik AR, Keshavarz A, Rajabi J, Hosseini Shokuh J. Evaluating outbreak of cutaneous Leishmaniasis in military personnel referring to the 554 military Zanjan Hospital in 2008. J Army Univ Med Sci Iran 2011;9:107-9.
Ullah S, Jan AH, Wazir SM, Ali N. Prevalence of cutaneous leishmaniasis in lower Dir District (NWFP), Pakistan. J Pak Assoc Dermatol 2009;19:212-5.
Rafati N, Shaporimoghadem A, Ghorbani R. Epidemiological study of cutaneous Leishmaniasis in Damghan (2000-2006). J Semnan Univ Med Sci 2007;24:250-1.
Roth-Damas P, Sempere-Manuel M, Mialaret-Lahiguera A, Fernández-García C, Gil-Tomás JJ, Colomina-Rodríguez J, et al.
Community outbreak of cutaneous leishmaniasis in La Ribera region of Valencia, Spain: Public health measures. Enferm Infecc Microbiol Clin 2017;35:338-43.
Himeidan YE, Abdel Hamid MM, Jones CM, Ranson H. Extensive permethrin and DDT resistance in anopheles arabiensis from eastern and central Sudan. Parasit Vectors 2011;4:154.
Abdallah H, Matamboa TS, Koekemoera LL, Mnzavae AP, Hunta RH, Coetzeea M. Insecticide susceptibility and vector status of natural populations of anopheles arabiensis from Sudan. Trans R Soc Trop Med Hyg 2008;102:263-71.
Hassan MM, Widaa SO, Osman OM, Numiary MS, Ibrahim MA, Abushama HM. Insecticide resistance in the sand fly, phlebotomus papatasi from Khartoum State, Sudan. Parasit Vectors 2012;5:46.
[Table 1], [Table 2], [Table 3]