Sequential Plasmodium Infections in Two Resident Families in Mangalore, India

doi:10.21203/rs.3.rs-4894618/v1

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Sequential Plasmodium Infections in Two Resident Families in Mangalore, India

https://doi.org/10.21203/rs.3.rs-4894618/v1

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Eleven members of two resident families in Mangalore city suffered from Plasmodium falciparum, P. vivax and mixed infections of both parasites in a sequential manner despite using bed nets regularly. Malarial symptoms of febrile illness started with chills and rigors at the schools for children and at work places for adult members. Five members of first family are from the central part of the city, and six members in the second family reside ∼10 km away from the central city, their live locations as well as community health care (CHC) center were mapped using QGIS software, respectively. Interestingly, first infection started with P. falciparum followed by P. vivax in the first family. However, P. vivax appeared first in the second family followed by mixed infection, and the last infection was P. falciparum. Both the families reside in close proximities of construction sites, which correlate with the role of mosquito breeding sites and indoor biting in ongoing malaria transmission in the city.

Infectious Diseases

Plasmodium falciparum

Plasmodium vivax

mixed infection

construction sites

malaria transmission

Malaria is one of the major public health problems in many parts of the tropical world. Severe forms of malaria are usually caused by Plasmodium falciparum infections [1]. However, mounting evidences in recent years supports the capacity of Plasmodium vivax also causes severe malaria [2]. In 2019, an estimated 229 million cases of malaria occurred worldwide and 409,000 peoples died from the disease. Twenty-nine countries accounted for 95% of malaria cases globally. India contributed 2% of total global burden [1]. Now, malaria in India is on the decline, and has aimed to eliminate this disease by 2030. To achieve this goal, it is important to understand the local malaria epidemiology for an effective elimination strategy [3]. Plasmodium infection within the family represents an important aspect of epidemiology to understand the local transmission dynamics [4]. Malaria cases were observed in two families residing in the Mangalore city. The Dakshina Kannada district headquarter, Mangalore is situated on the southwestern coastal of Karnataka, India [Figure 1]. The city has an average elevation of 45 m above from sea level having tropical climate with annual average temperature of 27°C, humidity above 78% (maximum 93% in July), and annual rainfall is around 3783 mm (95% of rainfall is during the monsoon) [5], which exhibits suitable environment to harbor high vector density and contribute to high incidences of malaria. The city is characterized with immigrants, migrant workers, travelers, which are involved in import-export profession, building constructions, roadways, railway track constructions, fishing and various business activities including tourism. All these factors contribute to high incidences of malaria in the Mangalore city and its surrounding areas. Malaria transmission in Mangalore city is perennial, occurs mostly during monsoon and post-monsoon periods, and is associated with building constructions that support breeding grounds for the urban malaria vector Anopheles stephensi [6]. Infection occurs mostly in the construction workers and families who live within a close proximity to the construction sites [7]. The local malaria cases are reported from urban Mangalore city as well as∼10 km areas around the city within 60 administrative wards. Several government and non-governmental organizations (NGO) as well as local volunteers are working together to spread awareness about malaria and providing case management facilities in the city [8]. This change in the malaria control operations in Mangalore [8] and National malaria control program [3] have led to a significant reduction in malaria transmission in Mangalore as well as in several other states of India. However, the use of bed nets or long-lasting insecticide treated nets (LLINs) under malaria control programs has led to a shift in mosquito biting to earlier hours of the evening [9], change the mosquito behavior [10] and late morning biting practice [11], which allows transmission on-going. In addition, construction sites are potential mosquitoes breeding places, and indoor biting contribute to malaria transmission that poses new challenges in malaria elimination [7].

Here, we report two families, who had prior knowledge of malaria and used bed nets regularly in the night contracted malaria on a sequential manner. The families lived in a close proximity to the construction sites and got infected with P. falciparum, P. vivax and mixed Plasmodium infections in a sequential manner. Adult members of the families worked as daily wage workers. Giemsa-stained thick and thin blood smears of all malaria patients were examined using Carl Zeiss Primo Star light microscope (Germany) by expert microscopists [12, 13] and infections were also confirmed by rapid diagnostic test (RDT) kits approved by the national malaria program [13, 16]. After confirmed diagnosis, intravenous blood (pre-treated) was collected to access biochemical and hematological parameters [14]. Serological tests were also performed to detect the presence of HIV, HCV and HBsAg levels [15]. Parasitaemia was also estimated on blood smears as described by WHO [16]. Two trained expert microscopists examined both thick and thin smears, and the senior expert (SKG) confirmed the final parasitaemia results.

All the cases were treated costless by the physicians at the Wenlock District Government Hospital, Mangalore [Figure 1] as per the treatment guidelines of National Vector Borne Disease Control Program (NVBDCP) [17]. All the patients were discharged on day 4 after confirming negative for Plasmodium infections. Medicines and food facilities were provided free of cost to each patient. Hospital stays and laboratory investigation charges were waived for below poverty line (BPL) patients, who were the study participants. For above poverty line (APL) patient’s, investigation charges were either discounted or waived by District Medical Superintend (DMO) of Wenlock Hospital, Mangalore. Local NGOs and private volunteers assisted with the patient’s essential needs. Each patient was followed-up weekly up to day 28 for P. vivax and day 42 for P. falciparum and mixed infections. Throughout the treatment and follow-up period and inconsistency between persistent bearing infections, there is no reinfection, recrudescence or relapse cases are seen in our two families study. The physical measurements, parasitological, serological test, hematological and biochemical values of the participants on admission are shown (Table 1). Details of follow-up and parasitaemia are presented (Table 2).

Table 1

Demographic, haematological and biochemical laboratory findings of two families at the time of admission
	Family – 1					Family − 2
Clinical Parameter	Case 1	Case 2	Case 3	Case 4	Case 5	Case 1	Case 2	Case 3	Case 4	Case 5	Case 6	Ref. Range
Age, year	40	12	10	14	50	4	6	12	11	32	37
Sex, male/female	Female	Female	Female	Male	Male	Female	Male	Female	Female	Female	Male
Weight, Kg	49.3	28.8	26	30.2	62	14.8	18.5	35	32	54	61.5
Height, Cm	160	114.3	106.6	153	166	63.5	78.7	129.5	124.4	158	162.5
Hemoglobin levels (g/dL) Packed Cell Volume (%)	12.8 43.7	12.3 47.7	12.4 38.2	12.5 38.7	14 45.2	10.8 32.3	10.4 30.6	12.5 38.3	10.1 30.3	12.8 40.6	15.8 50.5	13–17 M & 12–16 F 35–45
Total RBC counts (million/mm3)	5.77	4.97	4.76	4.73	4.23	4.58	3.97	4.46	3.69	4.75	5.54	4.0–6.0 million
Platelet counts (per µL)	93000	69000	103000	150000	99000	158000	160000	130000	95000	143000	157000	150000–4,10,000
Blood glucose (mg/dL)	48	68	96	70	94	119	91	100	99	99	110	80–130
Blood urea (mg/dL)	24	51	25	18.7	13.5	55	20	30	13	28.6	19.6	10–45
Serum creatinine (mg/dL)	0.81	1.93	0.7	0.73	0.87	0.4	0.2	0.6	0.5	0.79	1.1	0.4–1.4
Serum bilirubin (mg/dL)	1.04	23.7	1.51	0.6	1.3	1.01	1.69	0.83	1.29	1.76	1.54	0.3–1.2
AST, IU/L	114	47	18	25.6	99	58	28	22	27	37	79	5.0–40.0
ALT, IU/L	77.5	68.6	15	22.2	74	19	19.2	13	17	53.5	17	5.0–40.0
Alkaline phosphatase (IU/L)	508.2	314	133	593.8	404.5	100	135	138	180	478.8	290.5	40–129
Total protein levels (g/dL)	7.59	13.9	7.48	8.26	10.18	7.2	6.7	7.7	7	7.96	6.65	6.0–8.3
Albumin levels (g/dL)	4.53	5.03	4.25	4.99	5.04	3.4	4.66	3.9	5	4.41	4.3	3.2–5.5
Globulin levels (g/dL)	3.06	8.87	3.23	3.27	5.14	3.5	2.5	2	4.8	3.55	2.35	1.8–3.4

Table 2

Clinical follow-up for fever (°C) and parasitaemia (/µL)
Family-1	Test Report	Day 0	Day 1	Day 2	Day 3	Day 7	Day 14	Day 21	Day 28	Day 35	Day 42
Case 1	Parasitaemia (per µL)	15527	1054	52	0	0	0	0	0	0	0
Case 1	Temperature °C	39.1	37.4	37.8	37.4	37	37.2	37.2	36.9	37	36.9
Case 2	Parasitaemia (per µL)	16786	1880	88	0	0	0	0	0	0	0
Case 2	Temperature °C	38.6	37.9	37.6	37	37	36.8	37	37.4	37.2	37
Case 3	Parasitaemia (per µL)	14116	400	84	0	0	0	0	0	0	0
Case 3	Temperature °C	38.8	37.9	36.9	36.8	37	37.2	37.2	36.8	36.8	36.8
Case 4	Parasitaemia (per µL)	5036	349	16	0	0	0	0	0	Follow-up complete	Follow-up complete
Case 4	Temperature °C	38.4	37	37.4	37.6	37	37.2	37	37	nil	nil
Case 5	Parasitaemia (per µL)	4089	83	0	0	0	0	0	0	Follow-up complete	Follow-up complete
Case 5	Temperature °C	38.4	37	37.9	37.2	36.8	37	37.2	37	nil	nil
Family-2	Test Report	Day 0	Day 1	Day 2	Day 3	Day 7	Day 14	Day 21	Day 28	Day 35	Day 42
Case 1	Parasitaemia (per µL)	6345	317	73	0	0	0	0	0	Follow-up complete	Follow-up complete
Case 1	Temperature °C	38.5	37.6	37.2	37	37.2	37.2	37	37	nil	nil
Case 2	Parasitaemia (per µL)	13988	1389	888	0	0	0	0	0	0	0
Case 2	Temperature °C	38.8	37.6	37.4	37.2	37.2	37	37	37.2	37.2	37
Case 3	Parasitaemia (per µL)	4458	129	0	0	0	0	0	0	0	0
Case 3	Temperature °C	38.7	37	38.2	37	36.8	36.9	36.8	37	37.2	37
Case 4	Parasitaemia (per µL)	4079	267	0	0	0	0	0	0	0	0
Case 4	Temperature °C	38.5	37.2	37.2	37	36.8	36.9	37	37	37	37
Case 5	Parasitaemia (per µL)	5016	117	0	0	0	0	0	0	Follow-up complete	Follow-up complete
Case 5	Temperature °C	38.4	37.4	37.2	37	37.1	37.2	37.2	37	nil	nil
Case 6	Parasitaemia (per µL)	15508	1078	107	0	0	0	0	0	0	0
Case 6	Temperature °C	39.1	37.6	37.2	37	37.2	37	37.2	37.5	36.9	36.8

Using QGIS software, study area maps were generated by combining multiple images and maps, simplifying the mapping process and making it accessible for research purposes [Figure 1]. Open-source data from mapcruzin.com was utilized, specifically from GIS shapefiles.htm for specific features [18]. The complete dataset was accessed to provide a detailed overview of QGIS functionalities [19]. The use of QGIS for study area mapping demonstrates its value as an important GIS technique, and we encourage others to explore its applications for their specific research needs.

QGIS (version 3.22) was employed for spatial analysis [^1^]. Patients’ resident and Hospital location in map.

Family-1 Case Report

This family has lived in the city at Bunts Hostel, Mangalore for three decades, which is close to the Ponni Delta construction site. The family has five members including two males and three females (father, mother, son and two daughters). The parents were the main income source of the family and annual income depends on daily wage. The three siblings attended school in the nearby city.

Case No. 1

On 24.09.2015, the mother of the family (40-year-old) went for her daily work and visited the outpatient department (OPD) of the hospital. On physical examination, she was very sick and ill. Her blood pressure was 136/92 mmHg, pulse rate was 86 beats/minute, and temperature was 39.1°C. She also complained of headache, vomiting, anorexia and fatigue and was found positive for P. falciparum infection.

Case No. 2

The eldest daughter in the family (12-year-old) came to malaria clinic on 15.12.2015. On physical examination, the girl was very ill. Her blood pressure was 110/74 mmHg, pulse rate was 74 beats/minute, body temperature was 38.6°C. She also presented shivering, headache, nausea and myalgia. She was also found positive for P. falciparum infection.

Case No. 3

The youngest daughter in the family (10-year-old) was admitted to the hospital on 18.02.2016. Her blood pressure was 120/80 mm of Hg, pulses rate was 72 beats/minute and temperature was 38.8°C. She had a fever with headache, chills with rigors for 1 day. The blood test results were positive for P. falciparum infection.

Case No. 4

The eldest son in the family (14-year-old) came with the complaint of fever and shivering to the hospital on 24.04.2016. His blood pressure was 108/76 mmHg, pulse rate was 78 beats/minute, body temperature was 38.6°C, but he had complained of headache, nausea and myalgia. The blood tests confirmed the presence of P. vivax infection.

Case No. 5

The father in the family (50-year-old) was admitted to the hospital on 20.06.2016 from his workplace. He presented chills and severe headache. His blood pressure was 140/90 mmHg, pulse rate was 84 beats/minute and temperature was 38.4°C. Shivering, nausea and myalgia were also observed. He was found positive for P. vivax infection.

Family 2 Case History

The family had resided in Thokottu under Ullal PHC∼10 km from the main city for two decades, which is close to the Palma Citius construction site. The family has six members in a house with two males and four females (father, mother, son and three daughters). The parents were the only source of income and annual income depends on daily wage. Out of the four siblings, two attended school in the nearby city

Case No. 1

The youngest daughter in the family (4-year-old) attended the hospital with her parents on 18.04.2016 with a complaint of overnight cold and sweating for two days. The girl appeared acutely ill. Her blood pressure was 100/70 mmHg, pulse rate was 88 beats/minute and body temperature was 38.5°C. She was found positive for P. vivax infection.

Case No. 2

The youngest son in the family (6-year-old) visited the hospital on 21.04.2016 along with his parents. His blood pressure was 110/78 mmHg, pulse rate was 96 beats/minute, and body temperature was 38.8°C. He complained of fever with headache, chills with cough for 1 day. Blood examinations revealed positive for mixed P. falciparum and P. vivax infections.

Case No. 3

The eldest daughter in the family (12-year-old) returned from school with current fever and immediately visited the hospital on 22.04.2016. She had no other visible illness, her blood pressure was 120/80 mmHg, pulse rate was 74 beats/minute and temperature was 38.7°C. Blood examinations revealed the presence of P. falciparum infection after cross examination (when first microscopist failed to detect the parasite). The RDT result was P. falciparum came after 20 minutes with a clear dark band.

Case No. 4

The second daughter in the family (11-year-old) visited the hospital on 12.11.2016 with acute illness. Her blood pressure was 100/68 mmHg, pulse rate was 72 beats/minute and temperature were 38.5°C. Blood examinations confirmed the presence of P. falciparum infection.

Case No. 5

The mother in the family (32-year-old) came to the hospital on 12.02.2017 with general weakness and headache for 1 day. Her blood pressure was 132/90 mm of Hg, pulse rate was 86 beats/minute and body temperature was 38.4°C. Blood examinations confirmed the presence of P. vivax infection.

Case No. 6

The father in the family (37-year-old) was admitted to the hospital on 20.06.2017. He presented severe headache, fatigue and general weakness. His blood pressure was 90/70 mm of Hg, pulse rate was 70 beats/minute with high grade fever of 39.1°C. He also complained about vomiting and anorexia. Blood examinations revealed the presence of P. falciparum infection.

The two families were using bed nets regularly, but this could not protect them from the infective mosquito bites. This is possibly due to changing in feeding time of An. stephensi the main malaria vector in urban areas [6]. It has been observed that 30.4% of the local community use bed nets. The local health department provides the super-eminent and durable log lasting insecticide-treated nets (LLINs) to the high-risk groups mainly hotel staff, resident school children etc. [20].

Mangalore city has been a center for malaria, endemic for three decades and contributes almost 71.4% of malaria cases in the state [20]. The surge in malaria has been largely attributed to increase urbanization and vigorous construction activities that brought in migrant workers from other part of the country (Odisha, Jharkhand, West-Bengal and Northeast states) where malaria is endemic [21, 22]. The malaria control program was started by private medical practitioners in association with local medical colleges, Mangalore City Corporation (MCC) and District Administration. Thus, the Malaria Control Action Committee (MCAC) was constituted in 1995. With the relentless efforts of MCAC to control malaria in Mangalore, almost all hospital and private laboratories were encouraged to report malaria cases on a weekly basis [23]. For immediate malaria case management, five Fever Treatment Deports (FTDs)-cum-laboratories were established in which one of the laboratories is open in the evening hours (3pm – 8pm) for individuals who work as daily workers, so the malaria cases can be identified in these vulnerable worker groups. A Mobile FTD consisting of a health visitor and ANM (Auxiliary nurse midwife, commonly known as ANM) facility was made available for patients with malaria, and this team also visits construction sites within the city regularly. A hotline was also started to report malaria cases and its related symptoms at the Malaria Control Cell. The MCAC helped in improving inter-departmental coordination between health department and town planning department in the city for better implementation of enacted by-law, and a provision was made for the ‘Malaria Clause’ in the construction license. The builders who overlooked anti-larval measures were fined, and the construction license was temporarily suspended [23]. Now, ‘smart surveillance’ based on the digital handheld GPS-tagged mobile device for symptomatic individuals has been under operation in the city [8]. These efforts may allow malaria transmission under control and eventually might be eliminated by 2030. However, malaria cases found in the two families highlight the presence of weaknesses in the reporting system by the local health workers or ANMs. This can be due to unavailability of two family members at particular fixed point during the visit of state health workers or ANMs, the parents were at construction sites and the children were at school but not at home or vice-versa. To avoid such missing malaria cases, the MCAC can come up with a policy with more frequent visits to households, school campus and construction sites, if the goal is to eliminate local and focal malaria cases. Primary screening of malaria cases can be done by school teachers, construction supervisors and volunteers using RDTs as these require minimal training and resources. It will also help to detect asymptomatic and active malaria cases, which are unlikely to seek treatment and they are usually missed by passive surveillance while remaining infectious to mosquitoes, thus act as reservoirs of malaria transmission [24].

We present two families who lived in a close proximity to the construction sites were found consecutively infected with P. falciparum, P. vivax and mixed Plasmodium infections despite the use of bed nets, which signifies the role of mosquito breeding sites and indoor biting in ongoing malaria transmission in the city. Need to cross examine the suspected microscopic slides by at least two expert microscopists before declare negative or either positive or provide antimalarial medication.

Ethical statement

Written prior informed consent was obtained from all the study participant patients. The institutional review board of ICMR-National Institute of Malaria Research, New Delhi, India reviewed and approved the study (Ref. No-ECR/NIMR/EC/2012/39). The research and ethics committee of the Kasturba Medical College (KMC) under Manipal Academy of Higher Education, Mangalore, Karnataka, India, approved the study (Ref. No- IEC KMC MLR 03 16/49). All essential regulatory procedures were followed strictly.

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interests.

Author details

¹ICMR-National Institute of Malaria Research, New Delhi-110077, India; Dr. Benudhar Mukhi, Mobile: +91-8197119414, ORCID iD and link https://orcid.org/0000-0002-8772-1729, E-mail: [email protected]. ²Department of Biotechnology, Institute of Applied Sciences and Humanities, GLA University, Mathura, India; Prof. (Dr.) Himanshu Gupta, E-mail: [email protected]. ¹ICMR-National Institute of Malaria Research, New Delhi-110077, India; Dr. Anupkumar R. Anvikar, E-mail: [email protected]. ³ICMR-National Institute of Malaria Research, Field Unit, Bangalore − 562110, India; Professor (Dr.) Susanta Kumar Ghosh, E-mail: [email protected].

Funding

This study was supported from the Indian Council of Medical Research, New Delhi, India.

Authors' contributions

BM participated in fieldwork, collected clinical and epidemiological data, laboratory analyses and patient follow-ups. HG and AA participated in data interpretation and critically reviewed this article. SKG generated the resources. BM, HG and SKG wrote this manuscript and all authors reviewed and approved the final manuscript.

Acknowledgments

The authors acknowledge the staffs of Malaria Clinic, Doctors, Nurses of Regional Advanced Pediatric Care Center, at the Wenlock District Government Hospital, Mangalore, Karnataka, India and Mr. M.C Shenoy, Local volunteer, from Mangalore, Karnataka for their support to this clinical malaria two families observational study.

Availability of data and material

The data used in this study are archived with Dr. Benudhar Mukhi and available from them upon reasonable request.

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Sequential Plasmodium Infections in Two Resident Families in Mangalore, India

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Family 2 Case History

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