The public health response to a Plasmodium malariae outbreak in Penampang district, Sabah during a COVID-19 movement control order

Moyog sub-district has a land area of 364.68 km² and 25 km from the capital of Sabah, Kota Kinabalu city. The area is surrounded by dense forest. The weather is tropical, with a wet season from November to January. Most of the villagers are farmers. There are also agricultural and plantation based industries. Following the detection of P. malariae by real-time polymerase chain reaction (RT-PCR) from a blood sample of a farmer on 16^th July 2020 in this district, the Penampang District Health Office declared an outbreak of malaria in a village called Moyog, which is located in Moyog sub-district, Penampang district, Sabah state, Malaysia. Moyog sub-district has a land area of 364.68 km² and 25 km from the capital of Sabah, Kota Kinabalu city. The area is surrounded by dense forest. The weather is tropical, with a wet season from November to January. Most of the villagers are farmers. There are also agricultural and plantation based industries. On 10th July 2020 the blood sample from this primary case was sent to Kota Kinabalu Public Health Laboratory (KKPHL), from the Penampang Primary Health Clinic. According to the Ministry of Health Malaysia regulation, detection of a single introduced or imported human malaria case within a particular locality, is considered an outbreak [8].

Specifically, regarding P. malariae, an outbreak is deemed concluded when no additional cases of P. malariae are identified within a 120 day period [8]. Consequently, in order to ensure an effective public health response and curb further transmission, Penampang District Health Office organized teams to investigate, control, and manage the outbreak.

ACD was performed by collecting venous blood samples from residents of all villages within 2 km of Moyog village, and thick and thin blood film slides were prepared. This distance was determined based on the known flight range of Anopheles balabacensis mosquitoes, which is approximately 500 m [12]. Additionally, it takes into account the distances that communities typically traverse around the villages. The slides were observed by an expert malarial microscopist at Penampang District Health Office. All positive slides were sent to the KKPHL for confirmation of diagnosis by RT-PCR using a commercially available kit (abTES™ Malaria 5 realtime (RT)-PCR II kit, AITbiotech, Singapore).

The index case was defined as the first individual with malaria during the outbreak, and served as the origin of subsequent cases. The primary case refers to an individual who directly acquires the infection through mosquito bites and may contribute to its spread within the outbreak context [13]. Uncomplicated malaria was defined as symptomatic malaria without signs of severe malaria or evidence (clinical or laboratory) of vital organ dysfunction. Severe malaria was defined as presentation with any of the following: coma, metabolic acidosis, severe anaemia, hypoglycaemia, acute renal failure or acute pulmonary oedema [13].

A map of cases was created using Open Source Geographic Information System (QGIS). Global Administrative Areas (GADM) (https://​gadm.​org/​data.​html) data was used for administrative boundaries. Road data was obtained from OpenStreetMap Data Extracts (https://​download.​geofabrik.​de). Records from the Penampang District Health Office were used for each village's location information included in the district. The coordinates of houses of all cases were determined via GPS.

To assess the vector status and its potential to spread malaria in the affected areas, entomological investigations were carried out by six entomologists and 12 staff from the Entomology Unit of the Sabah State Health Department. They were supported by the Entomology Units from Penampang, and Kota Kinabalu District Health Office. The investigation was conducted from 22nd July to 18th September 2020, three days consecutively from 1800 to 2400 h in every locality. Mosquitoes were caught by the bare leg catch method within 20–50 m radius of the residences of malaria cases. Samples were collected from places where the ecology was conducive to Anopheles breeding, such as areas shaded by trees, rock pools near rivers, water-filled animal footprints, and ephemeral puddles [14]. Because An. balabacensis is the primary vector of malaria in Sabah [4], the mid-guts and salivary glands of this species were examined under a compound microscope (40 ×) for the presence of Plasmodium oocysts and sporozoites, respectively [15]. The parity rate of female mosquitoes was determined by classification based on the WHO malaria terminology as either nulliparous or parous [13]. Mosquito larvae were collected by dipping at potential breeding sites.

To understand beliefs and risk behaviour which might be responsible for malaria transmission, a survey was carried out with adult patients using interview approach by one of the authors (BH) (Additional File 1).

From 2010 to 2020, no P. knowlesi malaria nor human malaria cases were reported from this district. The outbreak occurred from 16th July 2020 through 14th November 2020 (Fig. 1). Thick and thin blood slides were prepared from samples obtained from all 5254 residents of the following villages (Table 1): Tadong Adong, Mongkusilad, Rugading, Mangkatadan, Notorus, Sosopon, Noungon, Kibunut, Ponombiran, Kuala Kibunut, Pangi, Babagon, Tampasak, Babagon Laut, Timpayasa, Timpangoh Laut, Tirig, Terian, and Moyog. Microscopy identified two villagers with P. knowlesi infection, and sixteen villagers with P. malariae infection. However, RT-PCR identified all the cases as infected with P. malariae only. A total of 18 cases of P. malariae were detected from the residents of the following villages: Sosopon, Moyog, Tadong Adong, Mangkatadan, Notorus, Terian, and Babagon Laut. The median parasitaemia level was 1622/µL (ranged 157–10,667/µL) (Table 1). All patients were Malaysian despite 353 smears from samples collected from Indonesian residents. More than 50% of them had been residing in Sabah for more than ten years, while only three of them had been in the village for more than five years. It is not known whether they visited their home country during their residency period.

The index case was a 55 year-old male who previously lived and worked in Nabire town in the Papua province of Indonesia. On the 21st January 2020, he had a fever preceded by shivering, which continued for a week. He visited a private clinic, Klinik Gresli, in Naribe. A rapid diagnostic test for malaria was done, which showed a negative result. In early February 2020, he was admitted to a private hospital, MRCC Siloam Hospital, for proper investigation and treatment. He was admitted for 12 days but the patient was not made aware of the diagnosis. Because of his medical condition, he returned to Malaysia on 8th March 2020. He visited the emergency department of Queen Elizabeth Hospital, Kota Kinabalu but since this hospital was designated as a COVID-19 hospital and considered him a non-serious case, he was referred to Penampang Primary Health Clinic for further evaluation and treatment. He made four visits to Penampang Primary Health Clinic for check up on the 14th May, 2nd June, 17th June, and 6th July 2020. He was treated symptomatically without any diagnostic investigation for malaria. He was diagnosed with P. malariae by ACD performed in July 2020 after the malaria outbreak was declared. He was diagnosed with P. malariae on 25th July 2021 and this was confirmed by RT-PCR.

The malaria affected villages are far away from urban areas. They are surrounded by dense forests and there are several nearby rivers. The patients are clustered into two groups due to the closer location of the villages where the patients reside (Fig. 2).

A total of 164 adult mosquitoes were captured; 13 of them were female Anopheles, 12 were An. balabacensis and one Anopheles tesselatus. No Plasmodium sp. was detected in An. balabacensis. In addition, 59% of An. balabacensis were parous. A total of 50 Anopheles spp. larvae were detected in ponds, puddles, and riverbeds. Among them 24 were An. balabacensis and 24 were Anopheles barbirostris larvae, but only one larva of each species of An. tesselatus and Anopheles hyrcanus grp.

It was found that 74.7% (n = 14/19) of the cases were exposed to malaria due to activities such as fishing and hunting during the night. It was found that except one, 16 of the malaria patients did not use insect repellent (Additional File 2). Only eight used long-sleeved shirts and trousers during outdoor activities, while nine did not. When there was fever nine of them did self-treatment while eight visited a health clinic. None of them used bed nets during sleeping at night. The reasons for not using bed net were as follows: not necessary (7), hot (3), not comfortable (3), no need (3), and did not like (1). Twelve of them were not aware of the activities which might cause them to get malaria, whereas only five of them were aware.